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Scientia Horticulturae 116 (2008) 2126


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Fertilization regulates soil enzymatic activity and fertility dynamics


in a cucumber field
Lijuan Yang a,b, Tianlai Li a,**, Fusheng Li c,*, J. Hugo Lemcoff d, Shabtai Cohen d
b

a
Key Laboratory of Horticulture in Liaoning, Shenyang Agricultural University, Shenyang, Liaoning 110161, China
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 with
cucumber (Cucumis sativus L.) and the relationship with yield and soil nutrient availability was assessed. Soil enzymatic activity, measured as
phosphatase, catalase, invertase and urease activities, decreased in the early growth stages of cucumber, but increased in the late ones, when plant
were 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 NH4+N and available P concentration, but negatively correlated with leaf N
and P concentration. Cucumber yield was also positively correlated with the soil enzymatic activity. Our results demonstrate that soil enzymatic
activity 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 biochemical
transformations involving organic residue decomposition and
nutrient cycling in soil (Martens et al., 1992; McLatchey and
Reddy, 1998). Land management and utilization methods, crop
species and cultivation systems etc. can affect soil enzymatic
activity. Thus, this parameter can be used as a sensitive index to
reveal changes of soil quality due to land management, and to
monitor soil microorganism activity related to soil nutrient
transformation. Yang et al. (2005) indicated that soil enzymatic
activity was lower with increasing soil depth, e.g. soil
enzymatic activity in the 010 cm layer was significantly
higher than that in the 1020 cm layer. Bergstrom and Monreal
(1998) studied the relationship between soil enzymatic activity
* 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

and ecological processes on a landscape scale using


geostatistics method and reported that the former parameter
has an important ecological meaning.
Many researchers have studied the effect of fertilization on
soil fertility by investigating soil enzymatic activity (e.g. Jia
et al., 2001; Liu, 2004). Martens et al. (1992) reported for a
long-term study that the addition of organic matter maintains
high levels of soil phosphatase activity. Giusquiani et al. (1994)
indicated, for a field experiment, that phosphatase activity
increased when the compost manure was added at rates between
90 and 270 t ha1. All these studies were mainly concentrated
on the static effect of soil type and fertilization on soil
microorganism and enzymatic activity, but few studies have
been conducted on the effects of fertilization on the dynamic
changes of soil enzymatic activity. Therefore, this study will
examine effects of different fertilizations on the variation of soil
enzymatic activity in different growth stages of cucumber
plants and their relationships with leaf nutrient and soil
available nutrient concentration. Information obtained should
help the development of a more rational fertilization in a
vegetable field in order to maintain high soil fertility and
increase yield.

22

L. Yang et al. / Scientia Horticulturae 116 (2008) 2126

2. Materials and methods


Cucumber (Cucumis sativus L. cv. changchun mici, a local
variety) was grown in meadow soil at the Experimental Station of
Shenyang Agricultural University, Shenyang, Liaoning (latitude
418310 N, longitude 1238240 E, altitude 51.6 m). Soil pH was 6.7,
organic matter content was 25.7 g kg1, total N was 1.29 g kg1,
total P was 1.76 g kg1, available N was 96.8 mg kg1 (i.e. alkali
hydrolytic N, 1 mol L1 NaOH hydrolysis), available P was
103 mg kg1 (0.5 mol L1 NaHCO3) and available K was
174 mg kg1 (1 mol L1 neutral NH4OAc).
Six fertilization treatments were applied, i.e. CK (no
fertilization), 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 m2 each, under a randomized block design. Partially
decomposed organic manure, N, P and K fertilizers were
applied as horse manure, urea, superphosphate and potassium
sulfate, at a rate of 22,500 kg ha1, 254 kg N ha1, 273 kg
P2O5 ha1 and 675 kg K2O ha1, respectively. The nutrient
contents of the manure were 33.6 g kg1 of organic matter,
9.20 g kg1 of total N, 6.27 g kg1 of total P2O5 and
4.23 g kg1 of total K2O, respectively. Organic manure, P
and K fertilizers were applied as basal fertilizer or manure. The
N fertilizer was splitted and applied at three different times: 1/3
as basal fertilizer, 1/3 was applied 30 DAT (days after
transplanting), and 1/3 was applied 50 DAT.
Thirty-two cucumber seedlings were planted in each plot on
May 13, 1999. After planting, surface soil (020 cm) and plant
materials were sampled on June 12th (EG, early growth period,
i.e. 29 DAT), July 8th (EMG, early-mid growth period, i.e. 56
DAT), July 22th (MLG, mid-late growth period, i.e. 70 DAT)
and August 9th (LG, late growth period, i.e. 90 DAT). The
experiment ended on August 13th, 1999.
Four enzymatic activities in soil were analyzed using air-dried
soil according to Yan (1988). Phosphatase was analyzed with
nitrophenyl phosphate disodium (PhOH mg g1, 37 8C, 24 h),
catalase with KMnO4 (0.1 mol L1 KMnO4 mg g1, 30 8C,
20 h), invertase with Na2S2O3 (0.05 mol L1Na2S2O3 mg g1,
37 8C, 24 h) and urease with pH 6.7 citrate acid buffering
solution (NH3N mg g1, 37 8C, 24 h).
Soil NH4+ and NO3 concentrations were analyzed using
fresh soil, and other nutrients using air-dried soil. Total N and P
in leaves were analyzed with oven-dried samples, 48 h at 70 8C.

Fig. 1. Cucumber yield (kg h m2) under different fertilization treatments. CK,
no fertilization; M, organic manure; MN, organic manure + N; MNP, organic
manure + NP; MNK, organic manure + NK; and MNPK, organic manure + NPK.

Soil and plant nutrients were analyzed with conventional


methods (Lu, 2000).
Analysis of variance (ANOVA) was performed with the
SPSS for Windows software package, and mean comparison
was 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 the
different fertilization treatments at P0.01 level (Fig. 1). Organic
manure combined with any of the mineral fertilizers had the
highest cucumber yield, while CK treatment the lowest. No
significant differences were registered among treatments that
include manure (Fig. 1).
3.2. Soil enzymatic activity
Soil enzymatic activity was affected by both fertilization and
seasonal change (Tables 1 and 2).
Fertilization effects: as shown in Table 1, mean values for the
whole growing season reflect an activity increase in soil
phosphatase when K or P were applied together with manure.
Soil catalase activity was reduced when organic manure was
applied with mineral fertilizers. Soil invertase activity was not
affected significantly by any of the treatments. Soil urease

Table 1
Soil enzymatic activity in different fertilization treatments during growing season of cucumber
Treatment

Phosphatase (mg g1)

Catalase (mg g1)

Invertase (mg g1)

Urease (mg g1)

CK
M
MN
MNK
MNP
MNPK

1.68  0.31ab
1.53  0.51b
1.61  0.36b
1.92  0.43a
1.93  0.58a
1.86  0.42ab

1.56  0.09a
1.58  0.13a
1.41  0.15b
1.48  0.07ab
1.44  0.05b
1.51  0.06ab

2.13  0.28a
2.01  0.56a
1.93  0.31a
2.11  0.30a
2.05  0.26a
2.15  0.40a

2.06  0.18b
2.09  0.27ab
1.79  0.29c
2.08  0.24b
2.07  0.29b
2.23  0.30a

CK, 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 P0.05 level with different letters, not significant at P0.05 level with the
same letters.

L. Yang et al. / Scientia Horticulturae 116 (2008) 2126

23

Table 2
Soil enzymatic activity in various growth stages of cucumber
Growth stage

Date

Phosphatase (mg g1)

Catalase (mg g1)

Invertase (mg g1)

Urease (mg g1)

Early growth
Early-mid growth
Mid-late growth
Late growth

29DAT
56DAT
70DAT
90DAT

1.15  0.20
2.12  0.18
1.81  0.17
1.87  0.32

1.40  0.05
1.59  0.07
1.51  0.04
1.48  0.16

1.64  0.21
2.45  0.11
2.00  0.10
2.16  0.18

1.71  0.13
2.28  0.15
2.21  0.16
2.01  0.20

c
a
b
b

c
a
ab
bc

c
a
b
b

c
a
a
b

Values represent mean  standard error (n = 18). Different letters in the same column indicate statistically significant differences at P0.05 level.

activity increased significantly in the MNPK treatment, but


decreased significantly when only N fertilizer was applied with
manure.
Ontogeny effects: All the soil enzymes activity was
significantly 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). A net decrease was observed towards
the end of the growing season (Table 2).
3.3. Soil nutrients
Soil NO3N concentration in EG (June 12th, 29 DAT) and
LG (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 the
vigorous vegetative and reproductive growth stage. Another
reason could be the high temperature and many rain events in

Shenyang region, China, in July, which can cause NO3N


leaching, thus reduce soil NO3N concentration. In LG stage,
mature plants with fewer flowers and fruits probably reduce N
uptake which can result in the accumulation of NO3N, as
decomposition of soil organic matter and manure continues.
Salinas-Garca et al. (2002) also reported that tillage diminishes
soil nitrate concentration, since the incorporation of crop residues
into soil accelerates the mineralization of organic matter, which
favored nitrate loss by percolation or uptake by weeds.
Soil NH4+N concentration increased from EG towards
EMG stage, and, except for the M treatment, decreased
afterwards in MLG (July 22th, 70 DAT) stage (Fig. 2B). No
clear pattern was observed late in LG stage.
Soil alkali hydrolytic N concentration does not show an
obvious changing trend in different fertilization treatments
(Fig. 2C). Only clear high values were observed at the end for
M and MN treatments.

Fig. 2. Soil available nutrient concentrations (mg kg1) 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.

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L. Yang et al. / Scientia Horticulturae 116 (2008) 2126

Fig. 3. Leaf N and leaf P concentrations (g kg1) 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.

Available soil P concentration varied slightly with time in


the non-P fertilized treatments (Fig. 2D). In the P fertilized
treatments, this parameter was higher, mainly at EMG stage.
3.4. Leaf nutrient concentrations
Leaf N concentration exhibited, in general, a reduction
tendency in most of the treatments, with a sharp decrease in M
treatment at EMG stage (Fig. 3A).
Leaf P concentration presented a well-defined inverted bell
shape curve in all cases (Fig. 3B). This changing trend of leaf P
concentration was probably more related to the rate of fruit
demand.
4. Discussion
Our results demonstrated that applied organic manure and
chemical fertilizers could greatly alter soil enzymatic activity.
Partially decomposed organic manure reduced soil enzymatic
activity in the EG stage but increased gradually in the LG stage.
In the first stage, the decomposition of manure consumed
abundant soil oxygen, leading probably to part of the soil
environment to become anaerobic and thus, to a reduction of
soil enzymatic activity (Zhang et al., 2005). Changes in soil
enzymatic activity during the growth stages of cucumber,
indicate that soil enzymatic activity was not only affected by
fertilization, but also affected by other soil factors, e.g. soil
temperature, humidity, root excretion and microbial activity,
etc. The activities of four enzymes reached the lowest value in
EG stage, the highest value in MLG stage, and decreased
gradually after LG stage. Verstraete (1977) also indicated that
soil enzymatic activity was the most active in the vigorous
growth stage. Because root activity was strong in the mid
growth stage, i.e. vigorous growth stage, the root-secreting
ability and type and amount of secretion probably increased.
Applying N fertilizer decreased soil enzyme activity in
various growth stages, but added P and K fertilizers increased
soil enzyme activity to some extent. For example, P and K
fertilizers significantly promoted phosphatase activity, which
contrasts with the results obtained by Zhao (1998) and Sun et al.

(2003), who concluded that P and K fertilizers reduced the


phosphatase activity of both brown fluvoaquic soil and grey
cinnamonic soil. Results indicated that there might have
significant difference in soil biochemical properties between
vegetable soil and other agricultural soils, which need to be
further studied. Because urea was hydrolyzed into CO2 and
NH3 by urease, its product, NH3, may consequently decrease
soil 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 with
applied organic manure combined into chemical fertilizer or
only chemical fertilizers were significantly higher than those of
no fertilization soil. Marinari et al. (2000) showed that a higher
level of dehydrogenase activity was observed in soil treated
with vermicompost and manure compared to soil treated with
mineral fertilizer. In this study, the combined effect of organic
manure and chemical fertilizer was also better than that of only
chemical fertilizers. Because biological energy matter such as
organic manure can supply available energy, thus it can
accelerate microorganism and enzyme cell multiplication to
improve organism and enzyme living environment and then to
increase 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 soil
enzymatic activity, and microbial biomass, but NH4+N
fertilizer caused a decrease of amidase and urease activities
related to N fertilizer cycle. In other studies, soil enzymatic
activity in the treatment of organic manure combined with N, P
and K fertilizers was higher than that of the treatment of only
manure or only chemical fertilizers (Geng et al., 2000; Lu et al.,
2001).
Crop growth and nutrient uptake largely depend on soil
fertility while soil fertility level is closely related to the type and
activity of soil enzymes (Jia et al., 2001; Liu, 2004; Qiu et al.,
2004). Thus, there is close relationship among soil enzymatic
activity, soil fertility and plant nutrient status. In this study, the
correlation between enzymatic activity and nutrient concentration in soil and plant was analyzed (Table 3). Results showed
that each enzymatic activity of soil and their total activities

L. Yang et al. / Scientia Horticulturae 116 (2008) 2126

25

Table 3
Correlation between soil and leaf nutrient concentration and soil enzymatic activity
Enzyme activity
Total enzyme
Phosphatase
Catalase
Invertase
Urease

Leaf total N
**

0.62
0.51*
0.42*
0.48*
0.63**

Leaf total P
**

0.73
0.60**
0.60**
0.66**
0.43*

Soil NO3N
0.37
0.21
0.61**
0.37
0.46*

Soil NH4+N
**

0.93
0.80**
0.69**
0.86**
0.86**

Soil alkali hydrolytic N


0.44
0.22
0.34
0.38
0.29

Soil available P
0.61**
0.44*
0.57**
0.59**
0.61**

Note: P0.01 = 0.515, P0.05 = 0.404. (**) and (*) indicate significant correlation with n = 24 at P < 0.01 and P < 0.05, respectively.

Table 4
Correlation between soil enzymatic activity, soil and leaf nutrient concentration and cucumber yield
Parameter

Total enzymatic activity

Phosphatase activity

Catalase activity

Invertase activity

Urease activity

Correlation coefficient
Parameter
Correlation coefficient

0.85**
Soil NO3N
0.35

0.66**
Soil NH4+N
0.78**

0.78**
Soil alkali hydrolytic N
0.63**

0.76**
Soil available P
0.78**

0.87**
Leaf total N
0.51*

Leaf total P
0.84**

Note: P0.01 = 0.515, P0.05 = 0.404, n = 24. (**) and (*) indicate significant correlation with n = 24 at P < 0.01 and P < 0.05, respectively.

were negatively correlated with leaf nutrient concentration. In


particular, soil urease and catalase activity were negatively
correlated with soil NO3N concentration. In addition, there
was positive correlation between soil enzymatic activities and
the concentrations of NH4+N and available P concentration at
P0.01 level, but there was no significant positive correlation
between soil enzymatic activity and alkali hydrolytic N
concentration.
Soil enzymatic activity can reflect the strength of
biochemical process in soil, and the rate of decomposition
and transformation of organic manure in soil was mainly
controlled by soil microbes and enzyme activities. When soil
microbes and enzymes activities were higher, organic manure
decomposed and transformed more quickly, and then released
more nutrients per unit time. The nutrients from the
decomposition and transformation of organic manure can be
maintained in an available form in soil, and thus can supply
plant growth and development needs. For example, urease acts
mostly specific in the hydrolysis of urea and can only hydrolyze
urea into NH3 and CO2. Phosphatase can hydrolyze some kind
of organic compounds containing P into inorganic P, which can
be absorbed and utilized by plants, thus soil enzyme activity
was positively correlated with soil available nutrients. Higher
soil fertility results in vigorous plants growth, strong roots
activity, vigorous metabolism and higher nutrients uptake, but
lead to the great rate of transformation and metabolism to form
yield and quality indices, thus negative correlation between leaf
nutrients concentrations and soil enzyme activity was found in
this study. Wang (1982) and Zhou (1983) indicated that
different type and amount of fertilizers directly affected soil
enzymatic activities, and then affected nutrient uptake by plant
roots. And soil enzymatic activities can indicate the function of
soil ecosystem because they can reflect the intensity and
direction of various biochemical processes occurred in soil, and
also correlate closely with soil fertility (Yang and Wang, 2002;
He et al., 2002). But Vogt and Asbjornsen (1995) indicated that
there was causal relationship between soil enzyme and other
soil properties.

Cucumber yield was positively correlated with total enzymatic activities of the four enzymes and each enzyme activity in
soil, soil NH4+N, alkali hydrolytic N and available P
concentrations at P0.01 level, but negatively correlated with leaf
N and P concentrations even at P0.05 level (Table 4), respectively.
The possible reason for this is that leaf nutrients were moved into
fruits in LG stage. And high levels of soil enzymes activity
accelerated the mineralization of organic matter in soil releasing
more essential nutrients such as N, P and S, required for better
plant growth and high yields. Verstraete (1977) indicated that
there were positive correlations between crop yield and soil
phosphatase, invertase and urease activities, respectively. Li
(1986) also reported that black soil enzymatic activity correlated
positively with corn yield. In this study, the highest correlation
coefficients were urease activity (R = 0.87) and total enzymatic
activities (R = 0.85). If cucumber yield is used for the index of
vegetable soil productivity, thus total enzymatic activities may
also be used for the index of vegetable soil productivity.
5. Conclusions
We found that enzymatic activity in vegetable field varied
greatly in different seasons, with higher activity during the
vigorous growth stage of cucumber, but lower activity during
the early and late growth stages. Different fertilizers also
affected the enzymatic activity in the soil. Soil enzymatic
activities decreased in the early growth stage but increased in
the late growth stage when treated with partially decomposed
horse manure.
Chemical N fertilizer could suppress the activities of soil
enzymes but P and K fertilizers increased such activities. The
activities of soil enzymes were positively correlated with
concentrations of soil NH4+N and available P concentration,
but negatively correlated with leaf N and P concentrations of
cucumber. There was also a positive correlation between
cucumber yield and soil enzymatic activity. Our results
demonstrate that soil activity can be an indicator for dynamic
changes of soil fertility.

26

L. Yang et al. / Scientia Horticulturae 116 (2008) 2126

Acknowledgements
We are grateful to the research grants from Liaoning PhD
Science Fund and Guangxi Education Department Project
(2006-26).
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