Bioaccumulation And Physiological Responses Of Nickel In Plants R.S.

Sengar* and Kalpana Sengara

CONTENT 1. Introduction 2. Nickel in the environment 3. Global cycle of nickel 4. Nickel accumulation in plants 4.1 Distribution of nickel in plant 4.2 Nickel and plant growth 4.3 Nickel and plant diseases 5. Summery 6. References

College of Biotechnology, Sardar Vallabh Bhai Patel University of Agriculture & Technology, Meerut-250110

Introduction
Heavy metals pollution, has become one of the most serious environmental problems because of increased discharge , their toxic properties and other adverse effects, particularly on water resources and users. These are released into the environment both naturally and through anthropogenic sources, even natural weathering of rocks and soils accounts for one-sixth of the total emission of metals like Nickel and chromium (Merin 1984). Many industrial wastes contain metals or their salts. These have been accumulating in the sediments of streams , lakes, rivers and soils for years. Heavy metals are particularly hazardous due to their persistent nature and biological half life . the inorganic aerosols containing a large number of such trace

elements constituent and important family of carcinogens and mutagens (Vohra 1975). These metals may act either synergistically or antagonistically on the aquatic biota, and insomer cases cause a decline in biotic diversity. Nickel is commonly found in surface water in low concentration and belong to the iron cobalt group of metals. It is an important constituent of alloy and also used as a catalyst in hydrogenation of vegetables oils. Nickel is readily taken up by the plants and animals. Plant leaves are the major sink for nickel. It is accumulated even in seeds and husk. Even low concentration of nickel is toxic to wide variety of plants (Mishra and Kar 1974). Thus, the movement of nickel in the ecosystem is of great concern to mankind. An attempt is, therefore, made to review the available studies on bioaccumulation of nickel in plants and its possible role in plant diseases. Nickel is a heavy metal, present in soil, water and air, usually in trace amounts. However, rapid industrialization and urbanization during the recent past have caused accumulation of Ni and many other trace elements in varied habitats where from the acquisition by the plants and their further transfer to human and animal population may affect the life forms

seriously. There are a number of reports of stimulation of growth in higher plants by low concentrations of Ni in the nutrient medium (Mishra and Kar, 1974; Stedman, 1968; Welch, 1981) based on the studies with nutritional requirement of some plants (Welch, 1981; Reinbothe and Mother Urea, 1980) several investigators had suggested that Ni was an essential micronutrient for plant growth although no conclusive evidences were provided. However, Browen et al. (1987) have demonstrated that Ni is an essential micronutrient for barley which failed to complete its life cycle in the absence of Ni and addition of Ni to the growth medium completely alleviated its deficiency symptoms. Nickel has been demonstrated to be associated as the metallic co-factor of urease from Jack bean (Canavalia ensiformis) seeds (Dixon et al., 1980b). this enzyme catalyses the hydrolytic cleavage of urea to ammonia and carbon dioxide and is widely distributed in higher plants (Welch 1981; Aschmann and Zasuski 1987; De Kock and Mutehell 1957; Pinamonti et al. 1997; Nandi et al. 1987; Halsteed et al. 1969; Sengar et al., 1998; Prasad et al. 1997 and Sengar et al. 2008). A Swedish Mineralogist Axel Fredrik Cronstedt (1751) first of all reported the discovery of a new element which was named as Nickel. Further discovery of electrode position of nickel by Boettgers in 1843 and later on commercial invention of electroplanting machine by Prime and company of Birmingham, Enland in 1844, led to the excessive use of Nickel. This is evident from the figures of Nickel shown in the following table as a consequence of cumulative addition of nickel into the atmosphere through human activities. It obvious from the table that both production and emission of nickel are increasing with advancement of time.The quantities of nickel observed in principal reservoirs of earth crust have been summarixed in following table (Table. 2).

Besides, the addition of nickel in atmosphere due to human activity and the presence of the same in various earths crust, there are several other sources of atmospheric nickel. Important sources of the presence of atmospheric nickel considered to exist mainly in the form of aerosols are presented in the following table (Table - 3). It was mentioned in Science congress (Sharma 1981) that a polluted environment is not congenial for creative ideas, innovative skills or the brilliant scientific discoveries. It hampers the aesthetic sense, degrades the values of the life and generates evils in our minds. Pollutants present in the soil and atmosphere adversely affecting the physiological functions of plants as well. Nickel in the environment The physical characteristics of nickel are given in Table 4 .In sedimentary rocks, the abundance of nickel depends on its behavior during weathering of rocks and sediment transport. In

common igneous and metamorphic rocks, most of the nickel resides in ferromagesium minerals, which are relatively susceptible to chemical weathering. However, even though nickel is soluble in ground water (ph < 6.6), it is not usually much mobile in the surfacial environ. The nickel released during the decomposition of ferromagnesian minerals is largely retained in the weathered profile in association with clay minerals (short 1961) and hydrous iron or manganese oxide (Jenne 1968). Gibbs (1973) reported that nearly 80 per cent of the nickel transported by Yokonb and Amazon rivers was either in the form of coating on sediments grains or

incorporated into the structures of detrital minerals , while about 15 per cent was contained in organic solids , and very little amount was carried either in solution or absorbed on inorganic

particles. Barber (1974) reported that nickel contents of sedimentary rocks were generally low and much of the nickel resides within a detrital clay component. In any event, nickel often resides in a sulphide mineral following lithification and diagnosis of the sediment.

Global cycle of nickel Human being represent a very important macrobiological agent in the present day biogeochemical cycle of nickel.The nickel pool in human biomass is estimated to be 4X 10
9

individual, and the mean nickel content of an average individual reported to be 10mg.The dietry nickel intake for the reference person has been given as 0.44 mg day -1(Synder 1975) which would extrapolate to 6.4X 10 8 g yr -1 for the entire human population. Martin and meybeck (1979) reported that the quantity of nickel assimilated annually by the fresh water biota (4x 10 9 g ) represent nearly 12 per cent of the total nickel reservoir in such ecosystem.gibbs (1977) concluded that in rivers, 70 per cent nickel lies in the form of coating on suspended particles, about 20 n per cent is bound to organic soild materials and only about 5 per cent in the form of solution or as absorbed materials. Other sources of nickel in the ocean include materials. Other sources of nickel in the ocean include atmospheric input (2.5 x 10 10 g yr -1), industrial and municipal waste discharge (0.38x 10 10 g yr -1) and outflux from

sediments from the nickel reservoir in the ocean (8.4 x 10 14 g yr -1). The input of nickel to the deep ocean (i.e atmospheric fallout plus river input of dissolved nickel) is 1.8 x 10 10 g yr-1 . the average residence time of nickel in the deep ocean is estimated to be 2.3 x 10 4 yr which the

wopuld be considerably shorter in nearshore zones. Hodge et al (1978) showed that residence time for

nickel in coastal water of southern California was only 19 yr. our

understanding of the biological pumps for nickel in the hydrosphere is tenous at best. From the planktonic biomass (1.1 x 10 10 g ) asnd uptake of nickel during gross production (18x 10 10 g yr -1), the residence time for nickel in marine biota is estimated to be about 22 days. The nickel cycle in the atmosphere is presented in fig1 the total emission of nickel from natural sources is 32x 10 6 kg yr -1 , about 70 percent of the annual rate (47 x 10 6 kg ) is contributed by the anthropogenic sources (Nriagu 1980). Volcanic actiuvities and wind erosion of soil particles each account for 409 to 50 poer cent of the air- borne nickel released from natural sources. The principal sources of pollutant nickel in air are fossil fuel combustion (28x 10 6 kg yr -1) and non-ferrous metal production (9.6 x 10 6 kg yr -1). If it is assumed that all the emitted nickel is uniformaly distributed to a height of 10 km and that the average residence time of nickel in atmosphere is 7-12 days, the average nickel concentration in the southern and northern hemisphere would be 0.1 and 0,5 ng m-3 , respectively (Nriagu 1980) the hydrospheric part of the nickel cycle is illustrated in fig 2 . Accurate data on nickel concentration in polar ice are apparently not available. The nickel burden of the fresh water (3.4 x 10 10 g ) is

insignificant , compared to the ocean (8.4 x 10 10 g) (Nriagu 1980).

Nickel accumulation in plants Nickel is usually absorbed in the ionic form (Ni ++) from the soil or solution culture (crooke 1954, do kock and Mitchell 1957). Its absorption by plants is regulated by (i) the soil properties, notably pH an d organic matter content (Vergnano 1953, Halstead et al 1969), and (ii) the total amount of nickel present in the soil (Masuda and Sato 1962, Roth et al 1971).Crooke (1954) reported that when nickel versenate in ionic form was supplied to oat, the level was 10 times

more than the control. Tests with mustered (brassica compestris) and tomato (lycopersicon esculentum) exhibited that divalent cations including Ni++, were not as strongly absorbed by

plants when chelated with ethylene diamine tetra acetic acid (EDTA) De Kock and Mitchell 1957). Mizuno (1967), and musuda and sato (1962) found that the soil ph value <5.6 favoured the absorption of nickel largely due to the fact that exchangeable nickel content of the soil increased with the increasing soil acidity.Mizuno (1967), Halstead et al . (1969) and Bruene et al (1982), reported that the application of lime to the acidic soil reduced the absorption of nickel by raising the soil pH.the increase in phosphate content of soiul and addition of gypsum in acidic soils enhance nickel absorption (Halstead et al 1969; Musuda and Sato 1962) While studying the translocation of nickel in xylem of tomato, cucumber (cucumis sativa), corn (zea mays), carrot (Daucus carota and peanut (Arachis hypogeal) , (Tiffin 1971) recorded nearly 85 per cent of the nickel as the cation, and the remaining 15 per cent was translocated as a negatively charged compound. In corn, cucumber, carrot and peanut, most of the nickel was translocated as a negatively charged compound. In the rootsap of peanut, essentially all nickel was bound to negatively charged compounds. Presumably, nickel was chelated by an organic anion (carrior) before translocation took place. Many factors are known to affect the translocation and subsequent accumulation of nickel in plants.Turina (1968) reported that higher soil temperature influenced the distribution of nickel in different parts of rye (secale cereale), wheat (Triticum aestivum), and corn, by increasing nickel translocation from roots to the leaves.Tokovio and Maiboroda (1963) reported that in wheat and corn , application of phosphorus fertilizers decreased the accumulation of nickel and other elements in plants, but the nitrogen fertilizers has a reverse effect. Le Riche (1968) concluded that in potato (solanum tuberosum), nickel eas more strongly concentrated in the tops than roots

when the plants were treated with sewage sludge of high nickel content.The accumulation was altogether lacking in the tubers. In hydrostemma motley and hydrilla verticilla, the uptake increased generally with increase in nickel concentration in the medium (lec et al 1984). The enrichment factor which relates the metal content in plants to the metal content in cultivated media, generally decreased with increasing metal concentrations.

Distribution of nickel in plant Nickel is differentially distributed in plant parts. In oat (avena sativa), leaves usually contained more nickel than stem (Vergnano 1953).Crooke and knight (1955) recorded initial increase in nickel content for first 30 days of experimentation on oat. Maksudav et al (1962) reported 10-30 ppm nickel in leaves and 10 ppm in root system of Artemisia scoparia. Paribook and kuznetsova (1963) reported that the high temperature of soil affected distribution of nickel in plant . The stem had a low concentration , compared to leaves. In apple (Malus sylvestis), shkuvaruk et al (1965) reported that root contained more nickel than shoots. Makrova and Aivazyan (1968) found that the nickel content of cultivated crop plants was less than the weeds grown in the same field. The difference may be due to selective absorption of nickel by different plant species. The content of nickel in some apple trees, growing on alluvial and brown soil was 2.5 ppm in flowers and 0.4 ppm in fruits (petrova and radenkov

1969).Srivastav (1987) while working on bioaccumulation of nickel around soyabean and vanaspati industries complex recorded 98.45 to 133.37 ppm nickel in the liquid effluent containing suspended impurities. In roots and shoot of Bermuda grass (Cynodon dactylon), the average concentration of nickel was 22.04 and 11.72 ppm, respectively. The nickel content in

sediments samples collected from effluent collection ditch varied from 132.40 to 143.56 ppm. While the nickel concentration in a sample of water from a hand pump in the factory area was 0.30 ppm, in canal water 1 km and 1.5 km downstream from the discharge point , it was 0.58 and 0.51 ppm , respectively. In soil , the concentration of nickel ranged from 49.95 ppm (field 1 km upstream from the discharge point ) to 119.79 ppm (irrigated land 1.5 km downstream from discharge point) . Nickel and plant growth Nickel has been reported as a growth stimulant and a retardant for a wide variety of plants. Moreover, at high concentration it has definite growth retarding effects. William (1960) reported that nickel inhibited growth in Anacystis, whereas it was essential for the optimal growth of chlorella vulgaris culture Chaney (1963) observed that when assimiable nickel was eliminated from the soil , the plant growth was vigorous. Biczek and Konarzewski (1968) reported that nickel significantly increased the elongation and fresh weight of hypocotyls in sunflower (Helianthus annus). Using wheat coleoptiles or pea stem as the test material, Ivanova and Bakurszhieva (1968) reported that 0.00058 to 0.58 ppm nickel slightly affected the growth, while in combination with gibberelic acid at 34.7 ppm or indole acetic acid at 17.5 ppm, nickel had stimulated synergistically the growth of wheat coleoptiles but not the growth of pea stem Tansybeaeva and polyanichko (1970) reported that presowing treatment of cotton (Gossypium sp.) seeds with 20 ppm NiSO4 solution for a period of 16-18 hr increased the seedling growth .Pais et al. (1970) reprted that the growth and development of chillies (capsicum frutescene) and tomato plant were stimulated by the application of nickel at a concentration < 1 ppm, while at >1 ppm , it was toxic to these species.

Inhibition of the growth of Chlorella spp. By nickel (0.1ppm) was reported by upitis et al .(1974) Flavin and Slaughter (1971) reprted inhibition of flagellar movement in Chlamydomonas reinhardic with 0.18 ppm nickel acetate. Skaar et al. (1974) reported that Phaeodactylum tricornutum remained unaffected by 0.5 ppm of nickel , and exhibited slight reduction in growth at 1.0 ppm concentration . Fezy et al (1979) while working on Navicula pelluculosa reported that under nickel stress, concentrations of 0.1 ppm nickel reduced the population growth rate by 50 per cent probably due to the presence of ionic nickel in the medium. Hollobaugh et al (1980) reported that 0.06 ppm nickel inhibited growth of thalassiobira aestivalus. In anacystis nidulans, Whitton and Shekata (1982) observed that the growth of wild type was inhibited by 0.16 ppm of nickel.

Nickel and plant diseases Excess nickel concentration cause several physiological disturbance, of which yellowing of leaves or chloresis usually followed by necrosis is the visual manifestation of toxicity (Hewitt 1948).The fundamental cause of chloresis has been attributed to the induced iron deficiency since application of iron salts to the chlorotic tissue had restored the green pigment. Vergnono and hunter (1953) concluded that though chloresis always preceeded by necrosis , the necrotic areas in older plants were sometimes completely surrounded by the tissues with normal green pigment . thus , when necrosis was developmed , it did not necessary occur in chlorotic leaves. Crooke et al (1954) and Crooke (1955) concluded that the degree of chloresis was essentially determined by the relative proportion of nickel and iron in the nutrient medium.chloresis was severe at a nickel: iron ratio of >6 and usually negligible at <1. Crooke and knight (1955)

obtained a positive correlation between the severity of chloresis and nickel : iron ratio, nickel: copper ratio has also been responsible for chloresis and necrosis in some plants. Mizuno (1968) concluded that nickel : copper ratio value about 1.0 resulted in chloresis and necrosis of leaves. The resistance of plants to nickel toxicity was reduced when nickel : iron and nickel : copper ratios were increased. There are some reports on the effect of nickel on the synthesis of chlorophyll in detached etiolated wheat (Wang et al. 1958, Wang and Waygood 1959) and rice (Oryza sativa) (kar 1972) leaves where nickel inhibited chlorophyll synthesis. Shkol nik and Smirnov (1970) recorded stunting in stem and leaf deformation in sunflower. Ishihara et al (1968) reported that the suppression of tree growth and chloresis could be alleviated by the application of molybdenum either as a foliar spray or by adding into the soil.

Summery Heavy metal pollution has become one of the serious environmental problems today. This review is an attempt to collect and collate the published studies on bioaccumulation of nickel in plants, its movement in the environment and possible consequence on the morphology and growth of the plants factors affecting distribution of nickel in plants and nickel in plant diseases have been examined critically. Nickel has significance as a nutritive as well as a potentially toxic element in the plants and environment. Nickel is a heavy metals, present in soil, water and air, usually in trace amounts. However, rapid industrialization and urbanization during the recent past have caused accumulation of Ni and many others trace elements in varied habitats where from the acquisition

by the plants and their further transfer to human and animal population may affect the life forms seriously. Adequate literature does not exist to understand fully the mechanism of action of Ni in plants, although it is an important environmental contaminant. Several important elements such as nitrogen, sulphure, phosphorous and metabolism of macro-molecules are untouched. The literature survey, however demonstrate that the growth of plants certainly responds to Ni which of course varies according to the species, concentration of Ni and also according to the soil nutrient composition. We all are aware that agriculture production in falling now a days and scientists engaged in this field are trying their best to investigate the several factors affecting the crop production. Few studies conducted on the adverse effect of pollutant like Nickel on the physiological functions of few plants. Adequate literature does not exist to understand fully the mechanism of action of Nickel in plants, although it is an important environmental contaminant. Several important elements such as N, S, P and metabolism of macro-molecules (Proteins, nucleic acid, etc.) are untouched. The literature survey, however demonstrates that the growth of plants certainly responds to Ni, which of course varies according to the species, concentration of Nickel and also according to the soil nutrient composition. Plant can not complete their life cycle without adequate Ni. Nickel cannot be replaced by Al, Cd for the growth of soybeans. This is, in conjunction with the findings that Ni is essential for cowpeas and produces beneficial growth responses in several plants species, suggests that Ni should be classified as a micronutrient element essential for higher plants.

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supplementary studies of heavy metal uptake by plants. Kali Briefe 16:271-291 Buczek J, Konarzewski Z (1968) Effect of metal ions on the indole acetic acid and EDTA induced elongation and water absorption of sunflower hypocotye pol.37:245-254 Chaney EJ (1963) Plants containing substantially no assimilated nickel cons, US 3, 107, 163 (cl. 71-1) oct . 15 , 1963, appl. may 28 , 1959 pp 3. Crooke WM (1954) Effect of nickel versenate on oak plants. Nature 173:403-404 Crook WM (1955) Further aspects of the relation between nickel toxicity and iron supply. Ann appl. Boil 43:465-476 Crooke WM, Knight AH (1955) The relation between nickel toxicity symptoms and the absorption of iron and nickel.Ann. Appl. Biol 43: 454-464 Crooke WM, Hunter JG, Vergnano O (1954) The relationships between nickel toxicity and iron supply.Ann. appl.biol.41:311-324 Do knock PC, Mitchell, RL (1957) Absorption of metal chelates by plants. Soil Sci 84: 55-62 Fenzy, JS Spencer, DF, Greene RW (1979) The effect of nickel on the growth of fresh water diatom-navicula pelliculosa env pollu (ser. B ) 20: 131-137 sections. Acta soc bot

Flavin M, Slaughter C (1974) Microtubule assembly and function in chlamydomonas inhibition of growth and flageller regeneration by antitubules and other drugs and isolation of resistant mutant. J. Bacteriology 118: 59-69. Austenfield FA (1979a) Phytotoxicity of nickel and cobalt on Phaseolus vulgaris cultivar saxa. Z. Pflanze. Nernaehr, Bodenkd. 142 (6): 786 791. Austenfield FA (1979b) Effects of nickel, cobalt and chromium on net photosynthesis of

primary and secondary leaves of Phaseolus vularis cultivar saxa. Photosynthetica. 13(4): 434 438.

Aschmann SG, Zasoski RJ (1987) Nickel and rubidium uptake by whole oat plant in solution culture. Physiol. Plant. 71: 191 196.

Banerji D, Kumar N (1979) The twin effect of growth promotion and heavy metal accumulation in certain crop plants by polluted irrigation water. Ind. J. Eco. 6(2): 82 87.

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Dixon NE, Blakely RL, B Zerner (1980) Back bean urease (Ec 3.5, 1.5) III. The envolvment of active site Nickel ion in inhibition by F - mercaptoethanol, phosphoramidate and fluoride. Ann. J. Biochem. 58: 481 488.

Gambi OVF, Cardini L, Pancaro R, Gabbrielle (1976) Effects of serpentine and nickel on some aspects of plant metabolism. G. Bot. Hal. Llo 415: 305 318.

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Table 1: Production and emission trend of nickel to the atmosphere in different years (Nariagu, 1980). Period Nickel production (x 109 kg) 1850 1900 1901 1910 1911 1920 1921 1930 1931 1940 1941 1950 1951 1960 1961 1970 1971 1980 1981 1990 1991 - 2000 All time total 0.20 0.14 0.33 0.36 0.83 1.37 2.38 4.37 7.07 8.09 9.06 34.15 Nickel emission to the atmosphere (x 109 kg) 12.0 8.2 21.00 21.00 49.00 80.00 140.00 257.00 415.00 446.00 464.00 10913.2

Table 2 Nickel in environment Reservoir Total (g) mass Average concentration (g/kg) Lakes and Rivers Total burden Plank tons Atmosphere Oceanic Dissolved Plants Consumers/ Reducers Suspended Particles Swamps and Marshes Biomass Terrestrial Biomass Plants Animals Litter Fossil Fuel Deposits Coal Oil shade Crude oil 10 x 1018 46 x 1018 0.23 x 1018 15 30 10 1.5 x 1014 1.4 x 1015 2.3 x 1012 2.4 x 1018 2.0 x 1016 2.2 x 1018 6.0 2.5 15.0 1.4 x 1013 5.0 x 1010 3.3 x 1013 1.4 x 1024 2.0 x 1014 3.0 x 1015 7.0 x 1016 6.0 x 1015 0.6 2.5 3.5 95.0 7.0 8.4 x 1014 5.0 x 108 1.1 x 1010 6.6 x 1012 4.2 x 1010 0.34 x 1020 5.7 x 1013 5.1 x 1018 1.0 4.0 0.3 3.4 x 1010 2.3 x 108 1.5 x 109 Nickel Reservoir (g)

Lithosphere (Down to 45 cm) Sedimentary Rocks Shale and Clay Lime Stone Sand Stone Organic Fraction

57 x 1024 2.5 x 1024 1.8 x 1024 0.35 x 1024 0.28 x 1024 6.8 x 1018

75 28 60 10 25 70

43 x 1020 1.2 x 1020 1.1 x 1020 0.04 x 1020 0.07 x 1024 4.8 x 1014

Table 3: Global values of Aerosol Production, Nickel Concentration in Particles and Nickel emission. Natural Sources Aerosol Production Nickel of Nickel (109 Kg/year) Nickel Emission

concentration in (106 Kg/Year) particles (PPM)

Soil Suspension Vegetation Forest Fires Meteoric Dust Seal Salt Total Anthropogenic Sources

120 75 12 0.0036 1000 World

40 11 15 50,000 0.009 -

4.80 0.82 0.19 0.18 0.009 8.5 (16%)

Nickel Emission Nickel Emission (106 Kg/Year)

Concumption (109 Factor Kg/year)

Fuel Oil

323

0.03 burned

Kg/ion 9.7

Residual Oil Municipal Incenerators Nickel

578 2550 0.002 burned 9 produced 0.24a 5 Kg/ion prduced 5 Kg/ion

17 Kg/ion 5.1

mining 0.80

Kg/ion 7.2

and refining Steel Production Transpiration Nickel production Coal burning 3300

1.2 0.9

alloy 0.14

Ni 0.70

charged 0.0002 burned Kg/ion 0.66

Cast production Copper

iron 0.03a

10

Kg/ion

Ni 0.30

charged Nickel 0.04a 1 Kg/ion Ni 0.40

alloy production Sewage sludge 48

charged 0.001 burned 43 (84%) Kg/ion 0.30

incineration Total

Where (a) indicates the amount of Nickel consumed in the activity

Table 4: Physical property of Nickel (Evenhort, J.L. 1971)

Characteristics

Value

Atomic number Atomic weight Boiling point Crystal structure Curic temperature Density of the met al g cm-3 General appearance Melting point Poisson s ratio Specific heat, 25 C

28 58 .71 D 2913 0 C Face centered cubic 353o C

8.90 Soft silvery metal 1455 0 C 0.31 0.106 cal. /gm

Fig 1 Global cycle of nickel in environment