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Chromium accumulation and toxicity in aquatic vascular plants

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Abstract

Chromium poisoning among leather tanners has long been known. The workers have been found to suffer from ulcers, allergic dermatitis, lung cancer, and liver necrosis due to prolonged contact with chromium salts. One of the highly catastrophic incidences of lung cancer as a result of inhaling dust containing Cr (VI) was reported in 1960 from the Kiryama factory of the Nippon-Denko concern on the island of Hokkaido, Japan.

Pollution of water resources, both surface and underground, by indiscriminate discharge of spent wastes of chromium-based industries has become a serious global concern, for it has created an acute scarcity of safe drinking water in many countries. In August 1975 it was observed that underground drinking water in Tokyo near the chromium (VI))-containing spoil heaps contained more than 2000 times the permissible limit of chromium. In Ludhiana and Chennai, India, chromium levels in underground water have been recorded at more than 12 mg/L and 550–1500 ppm/L, respectively.

Chromium is widely distributed in nature, occupying 21st position in the index of most commonly occurring elements in the earth’s crust. Chromium occurs in nature in the form of a compound (chromium + oxygen + iron) known as “chromite.” The geographical distribution of chromite mines is uneven. Over 95% of economically viable chromite ores are situated in the southern part of Africa. Its annual global production is ca. 9 million tons, mainly mined in the former Soviet Union, Albania, and Africa. In India, over 90% of chromite deposits are located in Sukinda Valley of Orissa.

Chromium occurs in several oxidation states, ranging from Cr2+ to Cr6+, with trivalent and hexavalent states being the most stable and common in the terrestrial environment. Chromium (III) is used for leather tanning because it forms stable complexes with amino groups in organic material. In the presence of excessive oxygen, chromium (III) oxidizes into Cr (VI), which is highly toxic and more soluble in water than are other forms. Chromium (VI) can easily cross the cell membrane, whereas the phosphate-sulphate carrier also transports the chromite anions. On the other hand, Cr (III) does not utilize any specific membrane carrier and hence enters into the cell through simple diffusion. The diffusion is possible only after the formation of appropriate lipophilic ligands.

Use of chromium as industrial material was discovered only 100 years ago. It was used for the first time in the production of corrosion-resistant steel (stainless steel) and coatings. Subsequently, chromium was widely deployed in various industries; namely, electroplating, dyes and pigments, textiles, photography, and wood processing. The tanning industry is one of the major users of chromium (III) salts. During leather processing the conversion of putrefactive proteinaceous matter, skin, into non-putricible is carried out by the treatment of chromium sulphate solution. According to an estimate, ca. 32 tons of chromium sulphate salts are used annually in Indian tanneries. As a result of unplanned disposal of spent tannery wastes, ca. 2000–3200 tons of chromium as element escapes into the environment. This has raised severe ecological concern and reduced the forest cover considerably.

Aquatic vascular plants play an important role in the uptake, storage, and recycling of metals. The uptake of metals depends on the chemical form present in the system and on the life form of the macrophytes (floating, free floating, well rooted, or rootless). The free-floating species (Eichhornia, Lemna, Pistia) absorb elements through the roots/leaves, whereas the rootless speciesCeratophyllum demersum absorbs mainly through the finally divided leaves.

Submerged species showed higher chromium accumulation than do floating and emergent ones. The order is:Elodea canadensis > Lagarosiphon major > Potamogeton crispes > Trapa natans > Phragmitis communis. Roots of water hyacinth (Eichhornia crassipes) showed an accumulation of 18.92 μmol (g dry tissue wt-1) Cr. AlthoughCeratophyllum demersum andHydrodictyon reticulatum showed lower levels of chromium accumulation, their bioconcentration factor values were very high.

Floating-species duckweeds (Lemna, Spirodela) are potential accumulators of heavy metals. They have bioconcentrated Fe and Cu, as high as 78 times their concentration in wastewater. Duckweeds have also shown the ability to accumulate chromium substantially. Although duckweeds attain higher concentrations of chromium in their tissues than do other macrophytes, their bioconcentration factor (BCF) values were much lower than those reported in other aquatic species.

A moderate accumulation of chromium has been found in emergent species. Plants ofScirpus validatus andCyperus esculentus accumulated 0.55 kg and 0.73 kg-1 Cr, respectively. InBacopa monnieri andScirpus lacustris accumulations of 1600 and 739 μg g-1 dw Cr, respectively, have been reported when exposed to 5 mg L-1 Cr for 168 hours in solution culture. The accumulation of Cr was greater in the root than the shoot. Higher accumulations of chromium in roots and least in shoots of emergent species have also been recorded.

Phytotoxicity of chromium in aquatic environment has not been studied in detail. The mechanism of injury in terms of ultrastructural organization, biochemical changes, and metabolic regulations has not been elucidated. It has been pointed out that while considering the toxicity of heavy metals, a distinction should be made between elements essential to plants and metals that have no proven beneficial biochemical effects. For example, an increased level of chromium may actually stimulate growth without being essential for any metabolic process. In aquatic species—namely,Myriophyllum spicatum— the maximum increase in shoot length was found at 50 μgl-1 Cr. Higher concentrations up to 1000 μ gl-1 caused an almost linear reduction both in shoot weight and length. Duckweeds showed relatively greater tolerance to chromium. However, an inhibition of growth inSpirodela andLemna was found at 0.02 mM and 0.00002 mM Cr concentrations, respectively. Mortality ofL. aequinoctialis was found at 0.005 mM Cr and higher concentrations. The effective chromium concentrations (EC-50) for some aquatic species have been reported as follows:Lemna minor, 5.0 mg L-1, 14 days EC;L. Paucicostata, 1.0 mg L-1, 20 days EC;Myriophyllum spicatum, 1.9 mg L-1, 32 days EC; andSpirodela polyrrhiza, 50 mg L-1, 14 days EC.

Chromium toxicity on biochemical parameters showed a reduction in photosynthetic rate at 50 μgl-1 Cr inMyriophyllum spicatum. Decrease in chlorophyll and protein contents were also recorded inNajas indica, Vallisneria spiralis, andAlternanthera sessilis with an increase in chromium concentration. InLimnanthemum cristatum, a slight reduction in chlorophyll and almost no change in control were found due to chromium toxicity. Submerged species (Ceratophyllum demersum, Vallisneria spiralis) and an emergent one (Alternanthera sessilis) showed decreases in chlorophyll as well as in protein contents when treated with chromium.

Chromium-induced morphological and ultrastructural changes have been reported in several aquatic vascular plants: InLemna minor andCeratophyllum demersum, chromium-induced changes in chloroplast fine structure disorganized thylakoids with loss of grain and caused formation of many vesicles in the chloroplast. Chromium (VI) has caused stunting and browning of roots produced from the chromium-treated excised leaves ofLimnanthemum cristatum. At 226 μg/g Cr dry wt leaf tissue concentration, development of brown coloration in the hydathodes of juvenile leaves ofLimnanthemum cristatum is a characteristic chromiuminduced alteration.

Aquatic vascular plants and algae may serve as effective bioindicators in respect to metals in aquatic environments. Chromium-induced morphological and ultrastructural changes inLimnanthemum cristatum have significant indicator values and could be used for assessing the level of chromium in ambient water.Wolffia globosa, a rootless duckweed, showed substantial chromium accumulation and high concentration factor (BCF) value at very low ambient chromium concentrations, suggesting its feasibility in detecting chromium pollution in water resources. Methylene blue-stained cells ofScenedesmus acutus become uniformly dark blue during chromium (VI) treatment. This may serve as an indicator of chromium pollution.

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Chandra, P., Kulshreshtha, K. Chromium accumulation and toxicity in aquatic vascular plants. Bot. Rev 70, 313–327 (2004). https://doi.org/10.1663/0006-8101(2004)070[0313:CAATIA]2.0.CO;2

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