Organic compounds with high Ni content: Effects on soil and strawberry production

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1 ISSN Revist Brsileir de Engenhri Agríol e Amientl v.2, n.8, p , 216 Cmpin Grnde, PB, UAEA/UFCG DOI: Orgni ompounds with high Ni ontent: Effets on soil nd strwerry prodution Luís F. Roved 1, Frnine L. Cuquel 2, Antônio C. V. Mott 3 & Vnder de F. Melo 3 1 Universidde Estdul do Prná/Cmpus Prnguá/Deprtmento de Ciênis Biológis. Prnguá, PR. E-mil: lfroved@gmil.om (Corresponding uthor) 2 Universidde Federl do Prná/Setor de Ciênis Agráris/Deprtmento de Fitoteni e Fitosnitrismo. Curiti, PR. E-mil: frnine@ufpr.r 3 Universidde Federl do Prná/Setor de Ciênis Agráris/Deprtmento de Solos e Engenhri Agríol. Curiti, PR. E-mil: ntonio.mott@pq.npq.r; vnderfm@ufpr.r Key words: hevy metls phytotoxiity iosolids residues A B S T R A C T The use of orgni residues n improve soil hemil nd physil onditions nd plnt growth. However, these residues often ontin hevy metls tht n interfere with growth. Here, pot experiment ws performed to ompre the effets of orgni ompound (OC) ontining high nikel (Ni) lod with those of minerl Ni soure (NiCl2, solule slt) on the prodution, qulity nd nutritionl sttus of strwerry nd on soil hemistry. Six dosges of Ni (, 9, 18, 36, 72 nd 144 mg kg -1 ) were dded to the soil using oth OC nd NiCl 2. The use of high-ni OC resulted in inresed produtivity nd fruit weight, wheres the solule NiCl 2 slt used redution in fruit weight. Applition of NiCl 2 t onentrtions >18 mg kg -1 lso used internervl hlorosis on leves, suggesting tht strwerry is highly sensitive to Ni. The minerl Ni soure ws lmost 15-fold more effetive thn the orgni soure t inresing lef Ni ontent. Applition of OC used n inrese of orgni mtter, C, sum of ses, tion exhnge pity, se sturtion, Zn, Mn, nd Cu, ut redued the levels of Mg in soil. Plvrs-hve: metis pesdos fitotoxidez iossólido resíduos Composto orgânio om ltos níveis de Ni: Efeitos no solo e n ultur de morngo R E S U M O O uso de resíduos orgânios pode promover não pens melhoris ns ondições químis e físis do solo e d plnt ms tmém entrd de metis pesdos no ilo iológio. Ojetivndo vlir o efeito de um omposto orgânio (CO) om ltos teores de níquel (Ni) e do loreto de Ni n produção, qulidde, nutrição do morngo e nos spetos químios do solo, onduziu-se um experimento em vsos. Aplirm-se seis doses de Ni, 9, 18, 36, 72 e 144 mg Ni kg -1 de solo por meio de um CO e um sl solúvel. Avlirm-se os efeitos n produtividde, qulidde de frutos e omposição quími (mro e mironutrientes) em teido d plnt tl omo efeitos no solo. A plição de CO om ltos teores de Ni proporionou umentos n produção e mss de frutos, porém o uso isoldo exereu derésimos n mss dos frutos; já n fonte minerl e ns miores doses provoou lorose internervl ns folhs. A ultur do morngo mostrou lt sensiilidde ns miores onentrções de Ni; enfim, o CO promoveu inrementos de MO, C, som de ses, CTC, sturção de se, Zn, Mn e Fe ms reduziu os teores de Mg. Ref Reeived 3 Jun, 215 Aepted 3 Jun, 216 Pulished 12 Jul, 216

2 Orgni ompounds with high Ni ontent: Effets on soil nd strwerry prodution 723 Introdution The use of sewge sludge, lone or in omintion with other orgni omposts (OC), inreses soil orgni mtter nd inorgni nutrients nd orrets soil ph (Boeht et l., 213). As result, sewge sludge hs een shown to improve plnt produtivity (Khn et l., 213). However, sewge sludge n lso inrese the levels of hevy metls suh s nikel (Ni) in the soil-plnt system (Pthk et l., 29). Nikel iovilility to plnts is omplex proess tht depends on the onentrtion nd hemil form of the metl nd on its intertion with other elements (Fuentes et l., 24). Orgni ompounds hve high ffinity to Ni nd derese its vilility y speifi dsorption (Yssen et l., 27). However, hnges in soil ph nd intertion with other hemils n use Ni to preipitte in soils, thus hnging its potentil ssimiltion y plnts (Misr & Pnde, 1974). The simple relese of Ni into the soil does not ensure its sorption y plnts (Rihrds et l., 1997), nd it is less dmging to plnts when omined with OC. Plnts lso hve mehnisms for mitigting Ni phytotoxiity y limiting its sorption nd redistriution, for exmple, free rdils tht n immoilize metls in the ell wll (Rihrds et l., 1997). Ni is onsidered n essentil plnt nutrient t low onentrtions (Wood et l., 26), ut t high onentrtions, Ni n interfere with the sorption of other ompounds, thus leding to physiologil dmge or plnt deth (Sengr et l., 28). Strwerry (Frgri x nnss Duh) rops hve high nutrient demnd nd strong potentil for the use of OC in its ultivtion. There re no pulished dt out the effets of Ni on strwerry. In this ontext, the im of this study ws to evlute the use of n OC with high Ni ontent on the qulity, prodution nd nutritionl sttus of strwerry plnts nd on the hemil hrteristis of the soil. Mteril nd Methods This experiment ws performed in April 29 t Cmpo Lrgo, Prná, Brzil ( S; W; 95 m.s.l.). The re is in mesotherml humid sutropil limte zone (Köppen s lssifition). The experiment ws onduted in open ir using 7.5-L pots (3 m dimeter) filled with Ineptisols (Ustepts) (USDA, 213). The soil ws extrted from 5 m depth in fllow re. Following homogeniztion, soil smple ws tken for nlysis of mro nd mironutrients ording to Cmrgo et l. (29), with the resulting vlues: ph (soil-wter), 4.4; P,.1 mg L -1 ; orgni mtter (OM), 4 g kg -1 ; se sturtion (V%), 2%. Clium (C, mmol L -1 ), 13; it ws determined s the sum of ses: K, 2; Mg, 6; H + Al, 15; nd tion exhnge pity (CEC), 126 mmol L -1. Boron (B) ontent ws.6 mg kg -1 ; opper (Cu) ws.95 mg kg -1 ; nd iron (Fe), mngnese (Mn), zin (Zn) nd Ni were 52, 1.25,.35, nd.37 mg kg -1, respetively. The soil ws orreted for ph (1 Mg h -1 of dolomiti limestone) nd enrihed with N, P 2 O 5 nd K 2 O (4, 26, nd 8 kg h -1, respetively). Soil orretion ws performed efore filling the pots nd pplying the tretments. The OC ws otined from petrohemil ompny lose to the experimentl re nd onsisted of residues produed in the industril re omined with sewge from the fility. The industril wstewter sludge ws treted y lkliztion with sodium hydroxide nd ws prtilly dried to produe doughy mteril (sewge sludge). This sludge ws then mixed with pine swdust (8:2 swdust:sludge), nd.8% ure ws dded to elerte the omposting proess. Composting ws used to redue the initilly high Ni onentrtion y dilution. However, the Ni onentrtion (72 mg kg -1 ) remined ove the legl limit of 42 mg kg -1 (CONAMA, 213). The omposting proess ws onduted in open ir for 6 months (18 d). Eight susmples of the omposted mteril were olleted nd mixed to form omposite smple, whih ws sent to the lortory for nlysis nd hd the following omposition: C/N, 17:8; ph (in wter) 7.6; density.5 g m -3 ; humidity 3.7%; OC, 87 g kg -1. Mronutrient ontents (g kg -1 ) were N, 4.9; P,.7; C, 68.7; Mg, 1.5; K, 1.9; nd S, 1.. Mironutrient ontents (mg kg -1 ) were s follows: B, 34.8; Cu, 2; Fe, 1; Cd,.5; Ni, 72 (whih orresponds to Ni: OM.72); Mn, 278; Zn, 234; P, 12; nd Cr, 23. The nlysis inluded digestion of the smples with nitri nd perhlori ids followed y hemil determintion using indutively oupled plsmtomi emission spetrometry (ICP-AES). Orgni mtter ws estimted y dry omustion through the evolution of roni dioxide. Nitrogen ontent ws determined y titrtion following digestion of the smple with sulfuri id nd distilltion of the resulting solution (Kjeldhl method). Phosphorus ws quntified y spetrosopy (Cmrgo et l., 29). To isolte the effet of Ni on the plnts, six experimentl dosges were pplied using OC (the orgni soure) nd solule Ni slt (NiCl 2, the minerl soure). The dosges were, 9, 18, 36, 72, nd 144 mg Ni kg soil -1, orresponding to OC pplition rtes of, 5, 1, 2, 4 nd 8 m 3 h -1, respetively. This followed the reommendtion of Brzilin environmentl genies (mximum onentrtion of 42 mg kg -1 or totl of 72 kg Ni h -1 ), so tht the first dosge levels were within the llowle onentrtion. The Ni dosges (from orgni nd minerl soures) were mixed into the soil to otin volume of 7.5 L, nd the mixture ws then dded to the pots for the plnting of strwerry seedlings. The experimentl design ws ompletely rndomized, inluding the two soures of Ni (orgni nd minerl), six dosge rtes nd four replites, with five plnts eh (one plnt per pot), for totl of 24 experimentl units. Strwerry (Frgri x nnss Duh Cmros ) ws plnted in eh pot nd mintined during the full experimentl yle (18 dys). Fertiliztion of surfe soil ws omplished y dding ure t rte of 4 kg h -1 in three pplitions, lulted on per-plnt sis. Produtivity ws estimted y ounting the totl numer of fruits nd estimting fruit weight per plnt. Hrvesting ws performed etween July nd Deemer, nd fruits t ommeril mturity stge (75% red epidermis) were olleted two to three times per week. In ddition, fruit qulity ws evluted t the eginning, middle nd end of the experimentl yle y rndomly seleting fruits, whih were slied nd entrifuged for their juie. The idity of the extrted juie R. Brs. Eng. Agrí. Amientl, v.2, n.8, p , 216.

3 724 Luís F. Roved et l. ws evluted y titrtion, nd solule solids were determined using refrtometer (AOAC, 25). The third nd fourth newly developed leves (without petioles) were olleted nd sujeted to hemil nlysis. Lef levels of C, Mg, K, P, Fe, Mn, Zn, B, Cu nd Ni were otined following lintion of the smples t 55 C nd soluiliztion in HCl (3 mol L -1 ). To nlyze nikel ontent, dry mtter (2.5 g) ws dry-digested nd the extrt ws filtered using one-qurter of the originl volume, thus inresing the onentrtion of the resulting solution eight-fold. Phosphorous ws determined y olorimetry nd totl C nd N were estimted y dry omustion. The remining hemils were determined with onventionl sorption spetrosopy using ir/etylene flme. At the end of the experiment, the soil ws homogenized to otin smples for nlysis of mro- nd mironutrients, ph, luminum, nd orgni mtter ording to the methods desried ove. Plnts were seprted, nd their roots, rowns nd eril prts were wshed, dried nd weighed to quntify dry mtter. The dt were nlyzed using nlysis of vrine. For signifint results, differenes in men vlues etween tretments were ssessed with Tukey tests (.5 signifine level) using regression models. A. 35 Fresh fruit plnt -1 (g) B. Fresh fruit (g) orgni soure minerl soure y = 1.38x R² =.88** y =-.4x x R² =.77* y =-.125x R² =.88** Dosge (Ni mg Kg -1 ) Different letters for the sme dosge indite signifint differenes (p <.5); * nd ** Signifint t.5 nd.1 levels Figure 1. Men produtivity per plnt (A); verge weight of fresh fruits in reltion to Ni dosges nd soures (B) Results nd Disussion A positive inrese in fruit prodution nd weight ws oserved for plnts treted with OC (Figure 1). In ontrst, in plnts treted with the minerl Ni soure, verge fruit weight deresed linerly, ut there ws no effet on produtivity. The numer of fruits ws not ffeted y the dosge or soure of Ni, nd the sme ws true for dry mtter, idity, nd solule solids. The inresed produtivity ws likely relted to the positive effets of the use of orgni residues, s demonstrted for other plnts (Khn et l., 213), nd my hve een relted to improvements in soil hemistry nd iophysil hrteristis. Thus, the high Ni lod of the OC used in this study pprently hd no negtive effets on strwerry prodution. The sme result ws found y Melo et l. (27), who ttriuted the sene of phytotoxi effets to omplexion of this hevy metl in their OC. The ddition of oth orgni nd minerl Ni soures to the soil resulted in liner inrese in its vilility (Figure 2). However, the orgni soure hd lower inrese ompred with the minerl soure. Levels of Ni in the leves hnged in reltion to soure nd dosge, with ler liner inrese with the pplition of minerl Ni, whih suggested muh higher vilility of Ni from this soure (Figure 2). Differenes in Ni vilility etween the soures my e relted to the higher speifi dsorption of orgni moleules, whih n limit hevy metl sorption y plnts (Vndenhove et l., 29), thus reduing the toxi effets of Ni in soil, even t high onentrtions. Aording to Misr & Pnde (1974), the ddition of orgni mtter to the soil resulted in soluiliztion of utohthonous Ni during the first few dys, due to the prodution of orgni ids tht led to omplexion of Ni with the orgni mtter, thus inresing its vilility to the plnts. A. Ni (mg kg -1 ) B. Ni (mg kg -1 ) orgni soure minerl soure orgni soure minerl soure Different letters for the sme dosge indite signifint differenes (p <.5); ** Signifint t the.1 level Figure 2. Nikel vilility in soil (extrted with DTPA) (A); Ni levels in strwerry leves s funtion of dosges nd soure of Ni dded to the soil (B) (minerl) y =.735x R² =.97** (ogrni) y =.49x R² =.99** y =.399x R² =.99** y =.27x R² =.9** Dosge (Ni mg kg -1 ) R. Brs. Eng. Agrí. Amientl, v.2, n.8, p , 216.

4 Orgni ompounds with high Ni ontent: Effets on soil nd strwerry prodution 725 In ontrst, the ddition of Ni vi minerl soure used stedy deline in verge fruit weight with inresing dosge (Figure 1), leding to smller fruits with lower mrket vlue. The vriility in produtivity ws ssoited with fruit weight. Mols & Brn (24) oserved phytotoxi effet of Ni delivered in solule soure, suggesting higher iovilility in this form. The lk of hnges in fruit idity nd solule solids ontent suggests tht fruit qulity ws not ffeted y the use of OC nd tht those prmeters re less suseptile thn produtivity. Similr effets were oserved y Hrgreves et l. (28), who found no differenes in fruit qulity in terms of solule solids etween orgni (i.e. orgni residues) nd trditionl systems. No phytotoxi effets were oserved when Ni ws delivered through the orgni soure. The omplexing effet of Ni ws exerted minly y orgni mtter ting s nturl multilinker to metls, eing held y the funtionl groups prtiipting in the intertion of orgni mteril x metl, whih re roxyli, phenoli, loholi, phenoli nd lso some of the ronyl group (Fuentes et l., 24), lso reported y Melo et l. (27). However, ler symptoms of toxiity, in the form of n internervl hlorosis in older leves, were deteted for the two highest Ni dosges from the minerl soure (Figure 3). These symptoms persisted until the leves were shed. Internervl hlorosis of strwerry leves (Figure 3) ws lso oserved y other reserhers (Pndey & Gopl, 21) nd my e linked to the toxiity of Ni. This hlorosis is due to depressed synthesis nd rpid oxidtive degrdtion of hloroplst pigments used y the Ni (Pndey & Gopl, 21). The verge Ni onentrtion in strwerry lef tissue reported y Mikiiuk & Mikiiuk (21) ws 2.8 mg kg -1. Wood et l. (26) found tht Ni ws toxi to rdish (Rphnus stivus L.) t onentrtions >12 mg kg -1 nd tht symptoms of Ni defiieny ourred in pen (Cry illinoensis Koh) t onentrtions of.5 mg kg -1. Thus, strwerry ws shown to e very sensitive to Ni, displying symptoms of toxiity t verge Ni onentrtions (5.9 mg kg -1 ) lower thn those found in other studies. On the other hnd, strwerry did not show symptoms of Ni defiieny t onentrtions <.5 mg kg -1, s found in pen (Wood et l., 26). The use of the orgni soure used inreses in most of the soil hemil hrteristis, inluding OM, C, SB, CEC, V%, Zn, Cu, nd Mn. The opposite ws found for H + Al nd Mg (Figure 4), nd there ws no effet on ph, P, or K (dt not shown). There ws no ler influene of OC pplition on Fe nd B vilility. In ontrst, the minerl soure hd no effet on ny of the hemil hrteristis. In tomtoes, Plios et l. (1998) found tht Ni restrited the sorption of P, inresed the sorption of K nd redued the sorption of Mg, Fe, Mn, Cu, nd Zn, with Mn displying the highest redution. Ni-indued hnges in the sorption of other nutrients re proly only expressed t higher levels of toxiity, when Ni n severely interfere with the sorption metolism. Those effets would not our if Ni onentrtions re lose to the tolerne limit of the speies, whih my prtilly explin these results. The enhned levels of orgni mtter in the soil (Figure 4) were diretly relted to the use of OC, s oserved in other A. B. Figure 3. Leflets of strwerry with symptoms of Ni toxiity (A); Helthy leflets (B) studies (Khn et l., 213). In ddition, inreses in orgni mtter ffet olloidl omplexes, reting stle moleules with high surfe hrge, whih normlly leds to signifint inrese in CEC in the soil (Pn et l., 23) s oserved here (Figure 4). Inreses in C, Mn, Cu, nd Zn (Figure 4) in soil were lso relted to the use of the OC. In ddition, inresed C ws refleted in the sum of ses nd se sturtion. Kidd et l. (27) found inresed C levels in soil nd ttriuted this to the high onentrtion of C used in the hemil stiliztion of the industril wstewter sludge used in their study. Other uthors lso reported inresed onentrtions of Zn, Mn, Fe, nd Cu in soil following the pplition of sewge sludge (Wrmn & Termeer, 25). The low vlues for potentil idity (H + Al, Figure 4) were relted to the retion of orgni moleules with the soil, ut were not relted to soil ph (dt not shown). The lk of hnges in ph ws proly result of the high ph (verge = 6.7) of the experimentl soil, euse the mendments were dded efore the seedlings were plnted. In ddition, ids produed during deomposition of the orgni mtter nd from nitrifition n limit the inrese in ph (Frnhini et l., 21). Deresed soil Mg levels in tretments tht reeived the orgni soure (Figure 4) were relted to the high onentrtions of tht element in the soil. Less soil ws required to ring pots ontining Ni from the orgni soure up to the experimentl volume (7.4 L), nd this might hve used the fll in Mg levels. In ontrst, Hshemimjd & Somrinti (211) found inresed soil Mg ontent when using OC. On the other hnd, the lk of effets on soil K onentrtions ws relted to the nturlly lower levels of this element in sewge sludge (Wrmn & Termeer, 25). In ddition, it is well estlished tht K hs high soluility in orgni omposts, whih my hve redued its onentrtion in soil y the end of the experiments. The OC pplition lso used smll hnges in nutrient onentrtions in the leves nd fruits, onentrtions were within the norml stndrd for the rop. There were inreses in the onentrtions of C, Mn, nd Zn in leves, nd inreses of Mg nd Zn nd dereses of K, Fe nd Cu in fruit (dt not shown). However, the hnge ws smll nd proly would hve little impt on plnt nutrition. R. Brs. Eng. Agrí. Amientl, v.2, n.8, p , 216.

5 726 Luís F. Roved et l A. B. 6 y =-1E-5x2 +.35x R² =.99** 5 (C) y =-.7x x R² =.99** 4 MO (g dm SB (mmol dm C. D. (SB) y = -.172x x R² =.99** 25 8 SB H+Al (H+Al) y = 4E-5x x R² =.73** H+Al (mmol dm Mg (mmol dm V (%) Mg C (Mg) y =.1x x R² =.99** V% CTC (CTC) y = -.5x x R² =.99** (V%) y = -3E-5x x R² =.78* C (mmol dm CTC (mmol dm Cu. Mn e Zn (mg dm E. F. Cu Mn Zn (Mn) y =.33x R² =.98** (Zn) y =-4E-6x 2 +.1x R² =.99** (Cu) y = 6E-7x 2 -.2x R² =.92** Fe (mg dm Fe B (B) y = 9E-8x 2-5E-5x +.73 R² =.81** (Fe) y = 5E-5x x R² =.62** B (mg kg -1 ) Dosge (Ni mg kg -1 ) Dosge (Ni mg kg -1 ) ** signifint t the.1 level; * signifint t the.5 level Figure 4. Men soil vlues of (A) OM, (B) C, Mg, (C) S, H + Al, (D) V%, CEC, (E) Cu, Mn, Zn nd (F) B nd Fe s funtion of inresing nikel dosges from the orgni soure Conlusions 1. The ddition of Ni vi OC pplied t onentrtions equl to nd 1.7- nd 3.8-fold higher thn the llowle limit led to inreses in strwerry fruit prodution nd weight, ut its use yielded dereses in fruit weight. 2. Ni delivered in minerl soure resulted in tissue Ni onentrtions up to 1-fold higher thn tht of Ni delivered in OC, nd the highest dosges used internervl hlorosis. 3. Addition of OC to the soil used inreses in OM, C, SB, CEC, V%, Zn, Mn, nd Cu, nd derese in Mg. Literture Cited AOAC - Assoition of Offiil Anlytil Chemists - Interntionl. Offiil methods of nlysis. 18. ed. Githersurg: AOAC, p. Boeht, C. L.; Sntos, J. A. J.; Aioly, A. M. de A. Net minerliztion of nitrogen nd soil hemil hnges with pplition of orgni wstes with 'Fermented Bokshi Compost'. At Sientirum. Agronomy, v.35, p , tsigron.v35i Cmrgo, O. A.; Moniz, A. C.; Jorge, J. A.; Vldres, J. M. A. S. Métodos de nlise quími, minerlógi e físi de solos do Instituto Agronômio de Cmpins. Cmpins: Instituto Agronômio p. CONAMA - Conselho Nionl do Meio Amiente. CT súde, snemento mientl e gestão de resíduos, GT regulndo o uso gríol de lodo de esgoto ( / onm/). 11 Dez Frnhini, J. C.; Gonzlez-Vil, F. J.; Crer, F.; Miyzw, M.; Pvn, M. A. Rpid trnsformtions of plnt wter-solule orgni ompounds in reltion to tion moiliztion in n id Oxisol. Plnt Soil, v.231, p.55-63, R. Brs. Eng. Agrí. Amientl, v.2, n.8, p , 216.

6 Orgni ompounds with high Ni ontent: Effets on soil nd strwerry prodution 727 Fuentes, A.; Llorens, M.; Sez, J.; Aguilr, M. I.; Ortuno, J. F.; Messeguer, V. F. 24. Phytotoxiity nd hevy metls speition of stilised sewge sludges. Journl of Hzrdous Mterils, v.18, p , Hrgreves, J. C.; Adl, M. S.; Wrmn, P. R.; Rupsinghe, V. H. P. The effets of orgni nd onventionl nutrient mendments on strwerry ultivtion: Fruit yield nd qulity. Journl of the Siene of Food nd Agriulture, v.88, p , dx.doi.org/1.12/jsf.3388 Hshemimjd, K.; Somrin, S. J. Contriution of orgni ulking mterils on hemil qulity of sewge sludge vermiompost. Ciêni e Agrotenologi, v.35, p , org/1.159/s Khn, S.; Wng, N.; Reid, B. J.; Freddo, A.; Ci, C. Redued ioumultion of PAHs y Ltu stuv L. grown in ontminted soil mended with sewge sludge nd sewge sludge derived iohr. Environmentl Pollution, v.175, p.64-68, Kidd, P. S.; Dominguez-Rodriguez, M. J.; Diez J.; Monterroso, C. Biovilility nd plnt umultion of hevy metls nd phosphorus in griulturl soils mended y long-term pplition of sewge sludge. Chemosphere, v.66, p , Mols, J.; Brn, S. Reltionship etween the hemil form of nikel pplied to the soil nd its uptke nd toxiity to rley plnts (Hordeum vulgre L.). Geoderm, v. 122, p , dx.doi.org/1.116/j.geoderm Melo, W. J. de.; Aguir, P. de S.; Melo, G. M. P. de.; Melo V. P. de. Nikel in tropil soil treted with sewge sludge nd ropped with mize in long-term field study. Soil Biology & Biohemistry, v.39, p , Mikiiuk, G.; Mikiiuk, M. Effet of polymer supersorent dded to medium on the ontent of minerl elements in strwerry leves nd fruit. Journl of Elementology, v.15, p , dx.doi.org/1.561/jelem Misr S. G.; Pnde, P. Effet of orgni mtter on vilility of nikel. Plnt Soil, v.4, p , BF1523 Plios, G.; Gómez, I.; Cronell-Brrhin, A.; Nvrro Pedreño, J.; Mtix, J. Effet of nikel onentrtion on tomto plnt nutrition nd dry mtter yield. Journl Plnt Nutrition, v.21, p , Pn, S. C.; Lin, C. C.; Tseng, D. H. Reusing sewge sludge sh s dsorent for opper removl from wstewter. Resoures, Conservtion nd Reyling, v.39, p.79-9, org/1.116/s (2)122-2 Pndey, V. K.; Gopl, R. Nikel toxiity effets on growth nd metolism of eggplnt. Interntionl Journl of Vegetle Siene, v.16, p , Pthk, A.; Dstidr, M. G.; Sreekrishnn, T. R. Biolehing of hevy metls from sewge sludge: A review. Journl of Environmentl Mngement, v.9, p , jenvmn Rihrds, B. K.; Peverly, J. H.; Steenhuis, T. S.; Lieowitz, B. N. Effets of proessing mode on tre elements in dewtered sludge produts. Journl of Environmentl Qulity, v.26, p , Sengr, R. S.; Gupt, S.; Gutm, M.; Shrm, A.; Sengr, K. Ourrene, uptke, umultion nd physiologil response of nikel in plnts nd its effets on environment. Reserh Journl of Phytohemistry, v.2, p.44-6, rjphyto USDA - United Sttes Deprtment of Agriulture. Soil Survey Stff, Nturl Resoures Conservtion Servie. Offiil soil series desriptions 2/6/ lssifition/osd/index.html. 12 Aug 213. Vndenhove, H.; Hees, M. V.; Olyslegers, G.; Vidl, M. Proposl for new est estimtes for the soil solid-liquid distriution oeffiient nd soil-to-plnt trnsfer of nikel. Journl of Environmentl Rdiotivity, v.1, p , jenvrd Wrmn, P. R.; Termeer, W. C. Evlution of sewge sludge, septi wste nd sludge ompost pplitions to orn nd forge: Yields nd N, P nd K ontent of rops nd soils. Bioresoure Tehnology, v.96, p , iorteh Wood, B. W.; Reilly, C. C.; Nyzepir, A. P. Field defiieny of nikel in trees: Symptoms nd uses. At Hortiulture, v.721, p.83-97, Yssen, A. A.; Bdrn, N. M.; Zghloul, S. M. Role of some orgni residues s tools for reduing hevy metls hzrd in plnt. World Journl Agriulturl Sienes, v.3, p.24-29, 27. R. Brs. Eng. Agrí. Amientl, v.2, n.8, p , 216.