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    Bioaccumulation And Physiological Responses Of Nickel In Plants

    R.S. Sengar*and Kalpana Sengar

    a

    CONTENT

    1. Introduction2. Nickel in the environment3. Global cycle of nickel4. Nickel accumulation in plants

    4.1 Distribution of nickel in plant

    4.2 Nickel and plant growth

    4.3 Nickel and plant diseases

    5. Summery6. References

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

    Meerut-250110

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    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

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    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).

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    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 108

    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

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

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

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    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

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    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

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    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 al1984). 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

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    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.

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    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 ofthalassiobira 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

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    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

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    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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    Reference

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    :273-280

    Bruce H, Ellinghaus R, Hetan J (1982) Heavy metal content of hessian soils and

    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 sections. Acta soc bot

    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

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    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 ofPhaseolus 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.

    Browen PH, Welch RM, Carry EE (1987) Nickel, a micronutrient essential for higher plants.

    Plant Physiol. 85: 801 803.

    Burton MAS, Lesuenr P, Puckett KJ (1981) Copper, nickel and thallium uptake by the lichen

    Cladina rangiferina. Can. J. Bot. 59 (1): 91 100.

    De Kock PC , Mitchell RL (1957) Absorption of metal chelates by plants. Soil Sci. 84: 55 62.

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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.

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    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.

    Gambi OV, Brooks RR, Redford CC (1979) Nickel accumulation by Italian spices ofAlyssum

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    stolonifera, Lunicera tatarica and Pinus resimosa. Can. J. Bot. 60: 2674 2681.

    Mishra D, M. Kar (1974) Nickel in plant growth and metabolism. Bot. Rev. 40: 395 452.

    Morgotti SP, Bravo F, Marre MT, Cocucci SM (1981) Effect of nickel ion on proton extrusion

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    Nandi S.K., R.C. Pant and P. Nissen (1987). Multiphasic uptake of phosphate by cor roots. Plant

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    Nriagn J.O. (ed.) (1980). Nickel in the environment. A Wiley interscience publication. John

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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)

    Nickel emission to the

    atmosphere (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

    0.20

    0.14

    0.33

    0.36

    0.83

    1.37

    2.38

    4.37

    7.07

    8.09

    9.06

    12.0

    8.2

    21.00

    21.00

    49.00

    80.00

    140.00

    257.00

    415.00

    446.00

    464.00

    All time total 34.15 10913.2

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    Table 2 Nickel in environment

    Reservoir Total mass

    (g)

    Average

    concentration

    (g/kg)

    Nickel

    Reservoir

    (g)

    Lakes and Rivers

    Total burden

    Plank tons

    Atmosphere

    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

    Oceanic

    Dissolved

    Plants

    Consumers/ Reducers

    Suspended Particles

    Swamps and Marshes Biomass

    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

    Terrestrial Biomass

    Plants

    Animals

    Litter

    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

    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

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    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

    of Nickel

    Aerosol Production

    (109

    Kg/year)

    Nickel

    concentration in

    particles (PPM)

    Nickel Emission

    (106

    Kg/Year)

    Soil Suspension 120 40 4.80

    Vegetation 75 11 0.82

    Forest Fires 12 15 0.19

    Meteoric Dust 0.0036 50,000 0.18

    Seal Salt 1000 0.009 0.009

    Total - - 8.5 (16%)

    Anthropogenic

    Sources

    World

    Concumption (109

    Kg/year)

    Nickel Emission

    Factor

    Nickel Emission

    (106

    Kg/Year)

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    Fuel Oil 323 0.03 Kg/ion

    burned

    9.7

    Residual Oil 578 17

    Municipal

    Incenerators

    2550 0.002 Kg/ion

    burned

    5.1

    Nickel mining

    and refining

    0.80 9 Kg/ion

    produced

    7.2

    Steel Production 0.24a 5 Kg/ion prduced 1.2

    Transpiration - - 0.9

    Nickel alloy

    production

    0.14 5 Kg/ion Ni

    charged

    0.70

    Coal burning 3300 0.0002 Kg/ion

    burned

    0.66

    Cast iron

    production

    0.03a

    10 Kg/ion Ni

    charged

    0.30

    Copper Nickel

    alloy production

    0.04a

    1 Kg/ion Ni

    charged

    0.40

    Sewage sludge

    incineration

    48 0.001 Kg/ion

    burned

    0.30

    Total - - 43 (84%)

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

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

    Characteristics Value

    Atomic number 28

    Atomic weight 58 .71 D

    Boiling point 29130C

    Crystal structure Face centered cubic

    Curic temperature353o C

    Density of the met al g cm-3

    8.90

    General appearance Soft silvery metal

    Melting point 14550C

    Poisson s ratio 0.31

    Specific heat, 25 C 0.106 cal. /gm

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    Fig 1 Global cycle of nickel in environment