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  Fertilization regulates soil enzymatic activity and fertility dynamicsin a cucumber field Lijuan Yang a,b , Tianlai Li a, **, Fusheng Li c, *, J. Hugo Lemcoff  d , Shabtai Cohen d a Key Laboratory of Horticulture in Liaoning, Shenyang Agricultural University, Shenyang, Liaoning 110161, China b College of Land Recourses and Environmental Science, Shenyang Agricultural University, Shenyang, Liaoning 110161, China c  Agricultural College, Guangxi University, Nanning, Guangxi 530005, China d  Institute of Soil, Water and Environmental Sciences, Volcani Center, Bet Dagan 50250, Israel Received 9 January 2007; received in revised form 12 July 2007; accepted 5 November 2007 Abstract Different fertilizers may affect soil enzymatic activity and soil fertility dynamics. These effects were investigated in a field experiment withcucumber ( Cucumis sativus  L.) and the relationship with yield and soil nutrient availability was assessed. Soil enzymatic activity, measured asphosphatase, catalase, invertase and urease activities, decreased in the early growth stages of cucumber, but increased in the late ones, when plantwere supplied with partially decomposed horse manure. Chemical N fertilizer inhibited soil enzymatic activity but P and K fertilizers enhanced it.Activity of different soil enzymes was positively correlated with soil NH 4+ –N and available P concentration, but negatively correlated with leaf Nand P concentration. Cucumber yield was also positively correlated with the soil enzymatic activity. Our results demonstrate that soil enzymaticactivity acted as a useful indicator of soil fertility dynamics. # 2008 Published by Elsevier B.V. Keywords:  Cucumber ( Cucumis sativus  L.); Fertilization; Soil nutrients; Soil enzymes; Soil fertility 1. Introduction Soil enzymes are derived primarily from soil fungi, bacteria,plant roots, microbial cells, plant and animal residues, etc.(Brown, 1973; Cao et al., 2003; Tarafdar and Marschner, 1994)and play a significant role in mediating biochemicaltransformations involving organic residue decomposition andnutrient cycling in soil (Martens et al., 1992; McLatchey andReddy, 1998). Land management and utilization methods, cropspecies and cultivation systems etc. can affect soil enzymaticactivity. Thus, this parameter can be used as a sensitive index toreveal changes of soil quality due to land management, and tomonitor soil microorganism activity related to soil nutrienttransformation. Yang et al. (2005) indicated that soil enzymaticactivity was lower with increasing soil depth, e.g. soilenzymatic activity in the 0–10 cm layer was significantlyhigher than that in the 10–20 cm layer. Bergstrom and Monreal(1998) studied the relationship between soil enzymatic activityand ecological processes on a landscape scale usinggeostatistics method and reported that the former parameterhas an important ecological meaning.Many researchers have studied the effect of fertilization onsoil fertility by investigating soil enzymatic activity (e.g. Jiaet al., 2001; Liu, 2004). Martens et al. (1992) reported for a long-term study that the addition of organic matter maintainshigh levels of soil phosphatase activity. Giusquiani et al. (1994)indicated, for a field experiment, that phosphatase activityincreasedwhenthecompostmanurewasaddedatratesbetween90 and 270 t ha  1 . All these studies were mainly concentratedon the static effect of soil type and fertilization on soilmicroorganism and enzymatic activity, but few studies havebeen conducted on the effects of fertilization on the dynamicchanges of soil enzymatic activity. Therefore, this study willexamineeffectsofdifferentfertilizationsonthevariationofsoilenzymatic activity in different growth stages of cucumberplants and their relationships with leaf nutrient and soilavailable nutrient concentration. Information obtained shouldhelp the development of a more rational fertilization in avegetable field in order to maintain high soil fertility andincrease yield. www.elsevier.com/locate/scihorti  Available online at www.sciencedirect.com Scientia Horticulturae 116 (2008) 21–26* Corresponding author. Fax: +86 771 3235314.** Corresponding author. Fax: +86 24 88421016. E-mail addresses:  tianlai@mail.sy.ln.cn (T. Li), zhenz@gxu.edu.cn (F. Li). 0304-4238/$ – see front matter # 2008 Published by Elsevier B.V.doi:10.1016/j.scienta.2007.11.001  2. Materials and methods Cucumber ( Cucumis sativus  L. cv. changchun mici, a localvariety)wasgrowninmeadowsoilattheExperimentalStationof Shenyang Agricultural University, Shenyang, Liaoning (latitude41 8 31 0 N, longitude 123 8 24 0 E, altitude 51.6 m). Soil pH was 6.7,organicmattercontentwas25.7 g kg  1 ,totalNwas1.29 g kg  1 ,totalPwas1.76 g kg  1 ,availableNwas96.8 mg kg  1 (i.e.alkalihydrolytic N, 1 mol L  1 NaOH hydrolysis), available P was103 mg kg  1 (0.5 mol L  1 NaHCO 3 ) and available K was174 mg kg  1 (1 mol L  1 neutral NH 4 OAc).Six fertilization treatments were applied, i.e. CK (nofertilization), M (organic manure), MN (organic manure + N),MNP (organic manure + NP), MNK (organic manure + NK)and MNPK (manure + NPK). Each treatment had three plots of 5 m 2 each, under a randomized block design. Partiallydecomposed organic manure, N, P and K fertilizers wereapplied as horse manure, urea, superphosphate and potassiumsulfate, at a rate of 22,500 kg ha  1 , 254 kg N ha  1 , 273 kgP 2 O 5  ha  1 and 675 kg K  2 O ha  1 , respectively. The nutrientcontents of the manure were 33.6 g kg  1 of organic matter,9.20 g kg  1 of total N, 6.27 g kg  1 of total P 2 O 5  and4.23 g kg  1 of total K  2 O, respectively. Organic manure, Pand K fertilizers were applied as basal fertilizer or manure. TheN fertilizer was splitted and applied at three different times: 1/3as basal fertilizer, 1/3 was applied 30 DAT (days aftertransplanting), and 1/3 was applied 50 DAT.Thirty-two cucumber seedlings were planted in each plot onMay 13, 1999. After planting, surface soil (0–20 cm) and plantmaterials were sampled on June 12th (EG, early growth period,i.e. 29 DAT), July 8th (EMG, early-mid growth period, i.e. 56DAT), July 22th (MLG, mid-late growth period, i.e. 70 DAT)and August 9th (LG, late growth period, i.e. 90 DAT). Theexperiment ended on August 13th, 1999.Fourenzymaticactivitiesinsoilwereanalyzedusingair-driedsoil according to Yan (1988). Phosphatase was analyzed withnitrophenyl phosphate disodium (PhOH mg g  1 , 37  8 C, 24 h),catalase with KMnO 4  (0.1 mol L  1 KMnO 4 m g g  1 , 30  8 C,20 h), invertase with Na 2 S 2 O 3  (0.05 mol L  1 Na 2 S 2 O 3 m g g  1 ,37  8 C, 24 h) and urease with pH 6.7 citrate acid bufferingsolution (NH 3 –N mg g  1 , 37  8 C, 24 h).Soil NH 4+ and NO 3  concentrations were analyzed usingfresh soil, and other nutrients using air-dried soil. Total N and Pinleaveswere analyzed with oven-driedsamples,48 hat70  8 C.Soil and plant nutrients were analyzed with conventionalmethods (Lu, 2000).Analysis of variance (ANOVA) was performed with theSPSS for Windows software package, and mean comparisonwas done using the least significant difference (LSD) test at  p < 0.01 or 0.05. 3. Results 3.1. Cucumber yield  There were significant differences in yield among thedifferent fertilization treatments at  P 0.01  level (Fig. 1). Organicmanure combined with any of the mineral fertilizers had thehighest cucumber yield, while CK treatment the lowest. Nosignificant differences were registered among treatments thatinclude manure (Fig. 1). 3.2. Soil enzymatic activity Soilenzymaticactivitywasaffectedbybothfertilizationandseasonal change (Tables 1 and 2).Fertilizationeffects:asshowninTable1,meanvaluesforthewhole growing season reflect an activity increase in soilphosphatase when K or P were applied together with manure.Soil catalase activity was reduced when organic manure wasapplied with mineral fertilizers. Soil invertase activity was notaffected significantly by any of the treatments. Soil urease Fig. 1. Cucumber yield (kg h m  2 ) under different fertilization treatments. CK,no fertilization; M, organic manure; MN, organic manure + N; MNP, organicmanure + NP;MNK,organicmanure + NK;andMNPK,organicmanure + NPK.Table 1Soil enzymatic activity in different fertilization treatments during growing season of cucumberTreatment Phosphatase (mg g  1 ) Catalase ( m g g  1 ) Invertase ( m g g  1 ) Urease (mg g  1 )CK 1.68  0.31ab 1.56  0.09a 2.13  0.28a 2.06  0.18bM 1.53  0.51b 1.58  0.13a 2.01  0.56a 2.09  0.27abMN 1.61  0.36b 1.41  0.15b 1.93  0.31a 1.79  0.29cMNK 1.92  0.43a 1.48  0.07ab 2.11  0.30a 2.08  0.24bMNP 1.93  0.58a 1.44  0.05b 2.05  0.26a 2.07  0.29bMNPK 1.86  0.42ab 1.51  0.06ab 2.15  0.40a 2.23  0.30aCK, no fertilization; M, organic manure; MN, organic manure + N; MNP, organic manure + NP; MNK, organic manure + NK; and MNPK, organic manure + NPK.Values represent mean  standard error ( n  = 12). Means in the same column are significant at  P 0.05  level with different letters, not significant at  P 0.05  level with thesame letters.  L. Yang et al./Scientia Horticulturae 116 (2008) 21–26  22  activity increased significantly in the MNPK treatment, butdecreased significantly when only N fertilizer was applied withmanure.Ontogeny effects: All the soil enzymes activity wassignificantly low at the early growth stage of cucumber (EG,June 12th, 29 DAT), but peaked at early-mid growth stage(EMG, July 8th,56 DAT). Anet decreasewasobservedtowardsthe end of the growing season (Table 2). 3.3. Soil nutrients Soil NO 3  –N concentration in EG (June 12th, 29 DAT) andLG (August 9th, 90 DAT) stages were higher than that of EMG(July 8th, 56 DAT) stage in different fertilization treatments(Fig. 2A). One reason could be high rate of N uptake during thevigorous vegetative and reproductive growth stage. Anotherreason could be the high temperature and many rain events inShenyang region, China, in July, which can cause NO 3  –Nleaching, thus reduce soil NO 3  –N concentration. In LG stage,mature plants with fewer flowers and fruits probably reduce Nuptake which can result in the accumulation of NO 3  –N, asdecomposition of soil organic matter and manure continues.Salinas-Garcı´a et al. (2002) also reported that tillage diminishessoilnitrateconcentration,sincetheincorporationofcropresiduesinto soil accelerates the mineralization of organic matter, whichfavored nitrate loss by percolation or uptake by weeds.Soil NH 4+ –N concentration increased from EG towardsEMG stage, and, except for the M treatment, decreasedafterwards in MLG (July 22th, 70 DAT) stage (Fig. 2B). Noclear pattern was observed late in LG stage.Soil alkali hydrolytic N concentration does not show anobvious changing trend in different fertilization treatments(Fig. 2C). Only clear high values were observed at the end forM and MN treatments. Fig. 2. Soil available nutrient concentrations (mg kg  1 ) during the growth stages of cucumber. CK, no fertilization; M, organic manure; MN, organic manure + N;MNP, organic manure + NP; MNK, organic manure + NK; and MNPK, organic manure + NPK.Table 2Soil enzymatic activity in various growth stages of cucumberGrowth stage Date Phosphatase (mg g  1 ) Catalase ( m g g  1 ) Invertase ( m g g  1 ) Urease (mg g  1 )Early growth 29DAT 1.15  0.20 c 1.40  0.05 c 1.64  0.21 c 1.71  0.13 cEarly-mid growth 56DAT 2.12  0.18 a 1.59  0.07 a 2.45  0.11 a 2.28  0.15 aMid-late growth 70DAT 1.81  0.17 b 1.51  0.04 ab 2.00  0.10 b 2.21  0.16 aLate growth 90DAT 1.87  0.32 b 1.48  0.16 bc 2.16  0.18 b 2.01  0.20 bValues represent mean  standard error ( n  = 18). Different letters in the same column indicate statistically significant differences at  P 0.05  level.  L. Yang et al./Scientia Horticulturae 116 (2008) 21–26   23  Available soil P concentration varied slightly with time inthe non-P fertilized treatments (Fig. 2D). In the P fertilizedtreatments, this parameter was higher, mainly at EMG stage. 3.4. Leaf nutrient concentrations Leaf N concentration exhibited, in general, a reductiontendency in most of the treatments, with a sharp decrease in Mtreatment at EMG stage (Fig. 3A).Leaf P concentration presented a well-defined inverted bellshape curve in all cases (Fig. 3B). This changing trend of leaf Pconcentration was probably more related to the rate of fruitdemand. 4. Discussion Our results demonstrated that applied organic manure andchemical fertilizers could greatly alter soil enzymatic activity.Partially decomposed organic manure reduced soil enzymaticactivity in the EG stage butincreased gradually in the LG stage.In the first stage, the decomposition of manure consumedabundant soil oxygen, leading probably to part of the soilenvironment to become anaerobic and thus, to a reduction of soil enzymatic activity (Zhang et al., 2005). Changes in soilenzymatic activity during the growth stages of cucumber,indicate that soil enzymatic activity was not only affected byfertilization, but also affected by other soil factors, e.g. soiltemperature, humidity, root excretion and microbial activity,etc. The activities of four enzymes reached the lowest value inEG stage, the highest value in MLG stage, and decreasedgradually after LG stage. Verstraete (1977) also indicated thatsoil enzymatic activity was the most active in the vigorousgrowth stage. Because root activity was strong in the midgrowth stage, i.e. vigorous growth stage, the root-secretingability and type and amount of secretion probably increased.Applying N fertilizer decreased soil enzyme activity invarious growth stages, but added P and K fertilizers increasedsoil enzyme activity to some extent. For example, P and K fertilizers significantly promoted phosphatase activity, whichcontrastswiththeresultsobtainedbyZhao(1998)andSunetal. (2003), who concluded that P and K fertilizers reduced thephosphatase activity of both brown fluvoaquic soil and greycinnamonic soil. Results indicated that there might havesignificant difference in soil biochemical properties betweenvegetable soil and other agricultural soils, which need to befurther studied. Because urea was hydrolyzed into CO 2  andNH 3  by urease, its product, NH 3 , may consequently decreasesoil enzymatic activity. In contrast, the products of P and K fertilizers should not inhibit soil enzymatic activity (Sun,1991). This is confirmed in our study.Qiu et al. (2004) indicated that soil enzymatic activities withapplied organic manure combined into chemical fertilizer oronly chemical fertilizers were significantly higher than those of no fertilization soil. Marinari et al. (2000) showed that a higherlevel of dehydrogenase activity was observed in soil treatedwith vermicompost and manure compared to soil treated withmineral fertilizer. In this study, the combined effect of organicmanure and chemical fertilizer was also better than that of onlychemical fertilizers. Because biological energy matter such asorganic manure can supply available energy, thus it canaccelerate microorganism and enzyme cell multiplication toimprove organism and enzyme living environment and then toincrease soil organism and enzyme composition and activity(Luo and Sun, 1994; Li et al., 2000). Dick (1988) indicated that long-term application of organic manure increased soilenzymatic activity, and microbial biomass, but NH 4+ –Nfertilizer caused a decrease of amidase and urease activitiesrelated to N fertilizer cycle. In other studies, soil enzymaticactivity in the treatment of organic manure combined with N, Pand K fertilizers was higher than that of the treatment of onlymanure or only chemical fertilizers (Geng et al., 2000; Lu et al.,2001).Crop growth and nutrient uptake largely depend on soilfertilitywhilesoilfertilityleveliscloselyrelatedtothetypeandactivity of soil enzymes (Jia et al., 2001; Liu, 2004; Qiu et al.,2004). Thus, there is close relationship among soil enzymaticactivity, soil fertility and plant nutrient status. In this study, thecorrelation between enzymatic activity and nutrient concentra-tion in soil and plant was analyzed (Table 3). Results showedthat each enzymatic activity of soil and their total activities Fig. 3. Leaf N and leaf P concentrations (g kg  1 ) during the growth stages of cucumber. CK, no fertilization; M, organic manure; MN, organic manure + N; MNP,organic manure + NP; MNK, organic manure + NK; and MNPK, organic manure + NPK.  L. Yang et al./Scientia Horticulturae 116 (2008) 21–26  24
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