effects of nutrient and pest management on soil microorganism in hybrid rice double‐annual...
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Effects of Nutrient andPest Management on SoilMicroorganism in HybridRice Double‐Annual CroppingSystemZeng Lu Sheng a , Liao Min a , Huang Chang Yong a &Subhani Abid aa Department of Resources Science , College ofEnvironmental and Resource Sciences, ZhejiangUniversity , Hangzhou, P.R. ChinaPublished online: 05 Feb 2007.
To cite this article: Zeng Lu Sheng , Liao Min , Huang Chang Yong & Subhani Abid(2005) Effects of Nutrient and Pest Management on Soil Microorganism in Hybrid RiceDouble‐Annual Cropping System , Communications in Soil Science and Plant Analysis,36:11-12, 1525-1536, DOI: 10.1081/CSS-200058508
To link to this article: http://dx.doi.org/10.1081/CSS-200058508
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Effects of Nutrient and Pest Managementon Soil Microorganism in Hybrid Rice
Double-Annual Cropping System
Zeng Lu Sheng, Liao Min, Huang Chang Yong, and Subhani Abid
Department of Resources Science, College of Environmental and
Resource Sciences, Zhejiang University, Hangzhou, P.R. China
Abstract: Combined effects on soil microbial activity of nutrient and pest management
in hybrid rice double-annual cropping system were studied. The results of a field experi-
ment demonstrated significant changes in soil phospholipid content, heterotrophic
bacteria, proteolytic bacteria, and electron transport system (ETS)/dehydrogenase
activity studied with different management practices and at different growth stages.
Marked depletions in the soil microbial biomass phospholipid contents were found
with the advancement of crop growth stages, while the incorporation of fertilizers
and/or pesticides also produced slight changes, lowest microbial biomass phospholipid
content was found with pesticides-alone application. A decline in the bacterial
abundance of heterotrophic bacteria and proteolytic bacteria was observed with the
continuance of crop growth, while lowest abundance of heterotrophic bacteria and pro-
teolytic bacteria were found with pesticides-alone application, which coincided with
the similar decline of soil microbial biomass. A consistent increase in ETS activity
was measured during the different crop growth stages of rice. The use of fertilizers
(NPK) alone or fertilizers and pesticides increased it, while a decline was noticed
with pesticides-alone application as compared with the control.
Keywords: Phospholipid content, heterotrophic bacteria, proteolytic bacteria, electron
transport system
Received 26 April 2004, Accepted 3 November 2004
Sino-Germany Cooperation Project on Agricultural Science and Technology, No.
2001-47.
Address correspondence to Liao Min, Department of Resources Science, College
of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310029,
P.R. China. Fax: 86-571-86971955; E-mail: [email protected]
Communications in Soil Science and Plant Analysis, 36: 1525–1536, 2005
Copyright # Taylor & Francis, Inc.
ISSN 0010-3624 print/1532-2416 online
DOI: 10.1081/CSS-200058508
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INTRODUCTION
Rice is the staple diet for approximately 30% of the world population and
for approximately 60% of the Asian population. This crop is preferentially
or generally cultivated under submerged soil conditions for better yields
and topographical situations (Sethunathan, Singh, and Raghu 1999). Soil
microorganisms constitute a large dynamic source and sink of nutrients in
all ecosystems and play a major role in plant-litter decomposition and
nutrient cycling (Collins, Rasmussen, and Douglas 1992), soil structure,
nitrogen fixation, mycorrhizal associations, reduction in plant pathogens,
and other alterations in soil properties influencing plant growth (Kennedy
and Smith 1995).
As intensively farmed agroecosystems that stay flooded for most of the
crop season, irrigated rice soils are unique in microbial ecology. Yet, a satis-
factory inventory of the microbial biomass in rice fields is still lacking. The
effects of submergence, crop stage, root environment, and agronomic
practices on the rice soil microbial community with its impact on nutrient
cycling have hardly been studied.
Evidence suggests that a distinct shift to the dominance of pesticide-
degrading aerobes after intensive use of a pesticide (diazinon and HCH
isomers) in flooded soil occurs due to the ability of the aerobes to utilize
the pesticide for growth as an energy source vis-a-vis cometabolism during
anaerobic transformation (Bhuyan et al. 1993). Thus, flooded soil serves as
an excellent medium for isolation of microorganisms, bacteria in particular,
with pesticide-degrading capabilities.
Studies of biodiversity and its relation to ecosystem structure and function
have focused primarily on macroorganisms, with little consideration of micro-
organisms, even though the latter perform key ecological roles (Parkinson and
Coleman 1991). Decomposition is dominated by microbial activities and is as
fundamental as primary production to the long-term functioning of ecosys-
tems. In addition, microorganisms are primarily responsible for the degra-
dation and detoxification of many environmental contaminants (Lamar and
Dietrich 1990). For these reasons, changes in the composition or activity of
microbial communities might have immediate or lasting effects on
ecosystem functioning (Perry et al. 1989).
Soil microorganisms are one of the most sensitive biological markers
available and are the most useful for classifying disturbed or contaminated
systems, since soil microbial activity can be affected by minute changes in
the ecosystem. The use of soil microbial activity for examination of
environmental stress and declining biological diversity needs to be investi-
gated more fully. In the present study, we studied the changes occurring in
soil microbial biomass, heterotrophic bacteria (copiotrophs and oligotrophs),
proteolytic bacteria, and their activity parameters in a paddy soil with
different nutrient and pest management in hybrid rice double-annual
cropping system.
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MATERIALS AND METHODS
Field Experiment
The experimental site was located around Jinhua city (29850 N, 1198470 E) in
the center of Zhejiang Province. This area has a subtropical climate with
annual rainfall of 1300–1500 mm and an annual mean temperature of
16.6–17.78C. The selected soil properties are listed in Table 1.
The treatments were control (without fertilizer and pesticides), NPK fer-
tilizers application (no pesticide), pesticides application (no fertilizer), appli-
cation of NPK fertilizers, and pesticides. The mineral fertilizer urea, calcium
perphosphate, and KCl were used at the rate of 100:25:100 kg/ha, respect-
ively. Pesticides included herbicides (butachlor and bensulfuron-methylþ
metsulfuron-methyl at field rate [FR] 4 days after transplanting [DAT]), insec-
ticides (triazophos, bisuta, and louprofezin at FR applied four times depending
upon pest occurrence), and fungicide (validamycin applied twice at FR). The
experiment was laid out according to randomized complete block design
(RCBD) with a plot size of 25 m2. All the treatments were replicated three
times, and the values appeared in the tables are their mean values expressed
on oven-dry-weight basis (1058C, 24 h).
Soil Sampling
The soil samples were taken at different growth stages of the rice crop (at
tillering, panicle initiation, and physiological maturity) in the standing
water or wet soil. Between rows and hills, 15 cm long cores were taken
using a (6 cm diameter � 20 cm length) rubber stoppered Plexiglass tube
equipped with a valve (6–8 cores/replicate), which was brought immediately
to the laboratory and used on the same day for the measurements of various
parameters.
Soil Analyses
Soil microbial biomass/total phospholipids (polar lipid fraction in lipids
extracted from soil) were determined by means of its phosphate content.
Table 1. Characteristics of the soil used
pH (H2O) 4.74 Cation exchange
capacity (cmolc kg21)
7.33
Water-holding capacity (g kg21) 510 Sand (g kg21) 278
Total organic carbon (g kg21) 15.25 Silt (g kg21) 562
Available N (mg kg21) 106.40 Clay (g kg21) 160
Available P (mg kg21) 13.34 Textural class Silt loam
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Inorganic O-phosphate is released by digestion of the lipid extract with
potassium persulfate, and color is developed by reaction of phosphate with
ammonium molybdate and malachite green and measured the absorbance at
610 nm (Frostegard, Tunlid, and Baath 1991). Viable counts of cultivable
heterotrophic bacteria were determined as colony forming units (CFUs) on
agar plates by the dilution plate method (James 1958; Reichardt 1978). Two
nutritional types, copiotrophs (heterotrophic bacteria adapted to high
nutrient concentration, “R-strategists”) and oligotrophs (with adaptation to
low nutrient concentrations, “k-strategists”) can be distinguished. For the enu-
meration of the copiotrophs, casein-peptone-starch (CPS) agar was used as the
plating medium (James 1958; Reichardt 1978). For the enumeration of the oli-
gotrophs, water-soil extract agar (SEA) was used as the plating medium
(James 1958). The samples were further serially diluted and suspensions
(150mL) spread in triplicate on to the CPS agar medium or SEA agar
medium. The plates were incubated at 308C, and copiotrophs were counted
after 4 days and oligotrophs after 4 weeks. Viable counts (CFUs) of
protein-degrading bacteria were done in the same way as previously
mentioned for heterotrophic bacteria. The suspensions (150mL) were spread
in triplicate onto the Gelatin-agar medium. The plates were incubated at
308C for 2 days and counted bacterial colonies with zones of clearing
(hydrolysis) that indicates proteolytic activity (Pitt and Dey 1970). Electron
transport system (ETS)/dehydrogenase activity was measured using
the reduction of 2-(p-iodophenyl-3-(p-nitrophenyl)-5-phenyl tetrazolium
chloride (INT) to iodonitrotetrazolium formazan (INT-formazan/INTF)
(Benefield, Howard, and Howard 1977). The absorbance values obtained
photometrically (480 nm) were converted to nmoles INT-formazan min21 g21
(dry soil) using a standard curve of INT-formazan (INTF).
Statistical Analyses
The experimental data were analyzed statistically according to completely
randomized design using CoStat Software. All measurements in this study
are the mean analysis of triplicate soil samples (CoStat 1990).
RESULTS
Effect of Nutrient and Pest Management on Soil Microbial
Biomass/Phospholipid Contents
The pesticides-alone application exerted a marked deleterious effect on the
soil microbial biomass phospholipid contents of the submerged paddy soil
as compared to the control, measured at different growth stages in both rice
crops (Table 2). A consistent and unambiguous decreasing tendency in the
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Table 2. Changes in microbial biomass phospholipid contents at various growth stages of rice under different treatments
Treatments
Crop I: Growth stages Crop II: Growth stages
Tillering Panicle Maturity Tillering Panicle Maturity
nmol phosphates g21 soil nmol phosphates g21 soil
Control 110.15 Aa 45.54 C 40.67 CD 50.64 B 33.26 C 19.53 EF
Fertilizer only 120.15 A 47.55 C 42.64 C 63.45 A 33.97 C 20.17 EF
Pesticide only 92.17 B 38.48 CD 29.97 D 31.24 CD 25.02 DE 16.71 F
Fertilizer and pesticide 114.69 A 42.04 C 39.58 CD 60.18 A 30.98 CD 19.81 EF
aMean values followed by the same letter (s) are not significantly different at P ¼ 0.01 based on Duncan’s Multiple Range Test.
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phospholipid contents was noticed with the passage of time at different growth
stages in both crops. The addition of fertilizer alone caused a slight and in most
cases nonsignificant improvement in the phospholipid contents as compared
with the control in all growth stages of both crops. Whereas, the combined
application of fertilizer and pesticide displayed mixed responses at different
growth stages probably due to variation in moisture status or input addition.
Comparatively lower phospholipid contents were estimated during all
growth stages of second crop than the first crop. The maximum quantities
of phospholipids that were recorded at tillering stage, in all the treatments
in both the crops, were gradually decreased in the next growth stage, and
the minimum phospholipid contents were observed in the last measured
stage. The submergence or anoxic soil condition caused marked depletion
in the microbial biomass phospholipid contents, which declined with time.
Effect of Nutrient and Pest Management on Soil Heterotrophic
Bacteria and Proteolytic Bacteria
Variations in bacterial counts at different growth stages of rice (proteolytic
bacteria for Crop I was not determined) were influenced by different treat-
ments (Table 3). An overall decrease in bacterial count was observed from
Crop I to Crop II and also in growth stages of both crops. The numbers of
colony-forming units in the submerged paddy soil were the highest at
tillering stage, which declined with progression of growth stage. Slight incre-
ments in few treatments were observed in heterotrophic bacteria at panicle
stage, against the tillering stage, which afterwards declined at maturity
stage. A distinct decreasing inclination in the proteolytic bacteria was
observed with the advancement of rice growth stage in various treatments.
Notable changes in the CFUs were also produced by the different treatments.
The maximum reduction in CFU counts was recorded with the application of
pesticides alone, while combined addition of fertilizer and pesticide and ferti-
lizer alone produced lesser depletions as compared to the control. The decline
in bacterial abundance (copiotrophs, oligotrophs, proteolytic bacteria) in the
field (Table 3) coincided with the similar decline of soil biomass as
measured by total phospholipids during a single cropping system.
Effect of Nutrient and Pest Management on ETS Activity
The ETS activity responded differently with different treatments at various
growth stages (Table 4). An overall increase in the ETS activity was
observed with the progression of growth stage in both crops of early and
late rice. The minimum ETS activity was recorded at the time of tillering in
all the treatments, which enhanced significantly (in few cases there was non-
significant increase) at panicle and maturity stages in both the rice crops taken
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Table 3. Changes in soil heterotrophic bacteria and proteolytic bacteria at various growth stages of rice under different treatments
Bacteria type Treatments
Crop I: Growth stages Crop II: Growth stages
Tillering Panicle Maturity Tillering Panicle Maturity
Copiotrophsb Control 6.1Aa 4.8C 4.2C 4.3A 4.0C 3.5B
Fertilizer only 4.6A 4.3C 4.1C 4.2A 3.9C 3.3B
Pesticide only 3.8B 3.4CD 2.8D 3.0B 3.5C 3.1BC
Fertilizer and pesticide 4.7A 4.0C 3.9CD 4.9A 3.8CD 3.5B
Oligotrophsc Control 4.8BC 4.7B 4.4C 4.5BC 4.3C 4.1CD
Fertilizer only 4.5BC 4.0BC 3.9BC 3.9BC 3.8CD 3.9CD
Pesticide only 4.0B 3.5C 3.4BC 3.4C 3.6CD 3.5D
Fertilizer and pesticide 4.8BC 4.4B 5.1C 5.0B 4.3CD 4.1CD
Proteolytic bacteriad Control 4.8A 4.5C 3.8CD 4.1B 3.8C 3.6C
Fertilizer only 4.6A 4.3C 3.9C 4.0B 3.8C 3.4C
Pesticide only 3.5B 3.1CD 2.8D 3.4C 3.2D 2.5D
Fertilizer and pesticide 3.9A 3.5C 3.2CD 3.7B 3.5CD 3.1CD
aMean values followed by the same letter (s) are not significantly different at P ¼ 0.01 based on Duncan’s Multiple Range Test.bCopiotrophs � 105.cOligotrophs � 104.dProteolytic bacteria � 103.
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Table 4. Changes in ETS activity at various growth stages of rice under different treatments
Treatments
Crop I: Growth stages Crop II: Growth stages
Tillering Panicle Maturity Tillering Panicle Maturity
nmol INTF min21 g21 soil nmol INTF min21 g21 soil
Control 135.8 EFa 220.4 D 358.5 B 123.6 D 129.3 D 307.4 B
Fertilizer only 159.6 E 266.1 C 450.9 A 154.2 D 237.2 BCD 421.7 A
Pesticide only 115.2 F 163.5 E 243.8 CD 112.8 D 134.1 D 170.1 D
Fertilizer and pesticide 142.7 EF 253.8 CD 414.2 A 133.6 D 183.6 CD 300.3 BC
aMean values followed by the same letter (s) are not significantly different at P ¼ 0.01 based on Duncan’s Multiple Range Test.
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(growth-stage effect). The different treatments also produced marked changes
in the ETS activity in both crops (treatment effect). Nearly similar responses
were recorded due to different inputs (fertilizers and/or pesticides) in two rice
crops. The application of fertilizers applied singly or in combination with pes-
ticides caused an increase in the ETS activity, while the addition of pesticides
alone declined it as compared to the control. The incorporation of fertilizers
alone and with pesticides at tillering stage enhanced the ETS activity by
17.5% and 5.1%, respectively, over the control. On the other hand, addition
of pesticides alone resulted in its depletion by 15.2% over control in
Crop I. The corresponding ETS values for panicle stage were found to be
20.7% and 15.1% higher (in fertilizer only and fertilizer and pesticide) and
25.8% lower (in pesticide), respectively, relative to the control. While at
maturity stage, these values further improved to 25.5 and 15.5 (increase),
and 32.0% (decrease), respectively, with reference to the control in Crop
I. Almost similar treatment response at various growth stages was recorded
in the second rice crop. Here, tillering and panicle stages, the difference
among treatments was found to be nonsignificant, while at maturity stage sig-
nificant changes were recorded. The pesticide used alone tended to decrease
ETS activity, while fertilizers alone or together with pesticides increased it
as compared to the control.
DISCUSSION
The wide range in soil microbial biomass, counts of bacteria, potential
activity, and biochemical parameters studied in the present investigation rep-
resents variations in soil microbial populations as a result of differences in
crop management.
Marked differences in the phospholipid contents of soil microbial biomass
were recorded at different crop growth stages, while incorporation of fertilizer
and/or pesticide also produced some changes. Phospholipids occur in the cell
membranes of all living cells and are not used as storage products (Petersen
et al. 1991). They are rapidly transformed into glycolipids after cell death.
Total phospholipids are therefore considered as an accurate measure of total
biomass of living microorganisms (Inubushi, Brookes, and Jenkinson 1991).
Earlier it has been observed that soil under aerobic condition contains larger
amounts of phospholipids than under facultative-anaerobic and anaerobic con-
ditions (Wingfield, Davies, and Greaves 1977). Slightly lower quantities of
phospholipids in pesticide-treated soils than in control soil might be due to
their toxicity (Wingfield et al. 1977). A notable depletion in biomass phospho-
lipid contents was also noticed by Reichardt et al. (1997) due to reduced
(anoxic) conditions in continuously cropped irrigated rice fields. The results
of the present field study are similar to the findings of the laboratory experi-
ments conducted under almost similar but controlled conditions (Subhani
et al. 2001). The slight fluctuations in the present field study at some places
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might be due to fluctuations in moisture, temperature, and additions of
different inputs during the crop growth.
The decline in bacterial abundance (copiotrophs, oligotrophs, proteolytic
bacteria) in the field coincided with the similar decline of soil biomass (as
measured by total phospholipids) during a single cropping system (rice
Crops I and II). This reduction can be explained by an exhaustion of energy
and nutrient carriers, a sudden increase of grazers (Clarholm 1994), a
drastic change in the redox regime, or a combination of these. The develop-
ment of microbial populations in soils grown to rice has scarcely been inves-
tigated. Nevertheless, a steep decline from the seedling to the flowering stage
has already been observed before, although field conditions and methodology
were different (Goshal and Singh 1995). Oxygen concentrations and diffusion
rates significantly affect the growth and respiration of soil bacteria. They may
have pronounced effects on the specific growth rate, maximum growth rate,
respiration, numbers and types of bacteria isolated from soil (Nagatsuka and
Furusaka 1980). Similar declines in direct microscopic count of bacteria,
and fungi were observed by investigators in a long-term intensive cropping
field experiment at the International Rice Research Institute farm and in
a greenhouse experiment employing the submergence-tolerant variety
(Subhani et al. 2000). They further reported that this decline in total
bacterial abundance in the field was matched with a similar decline of total
soil biomass (total phospholipids) (Reichardt et al. 1996). Conversely,
Reichardt et al. (1997) found an increase in viable counts of sulfate-
reducing bacteria, of total heterotrophic copiotrophs, and in concentrations
of diether lipids as fingerprints of methanogenic bacteria toward physiological
maturity of the rice crop. This finding contrasts with the general declining
trend, but they interpreted it as a gradual adaptation to the anoxic conditions
prevailing in the waterlogged crop soil. On the other hand, they observed that
proteolytic bacteria declined from the beginning of the cropping cycle on, as
was observed in the present study (Reichardt et al. 1997). They concluded that
the organic matter drives the buildup of microbial biomass pool by “copio-
trophic producers,” which is available as energy and as a carbon source in
the soil. Decline in the heterotrophic bacteria in the present study might be
due to the inadequate supply of energy and carbon source through organic
matter in the soil and due to some stress from different inputs that were
applied at different times during the crop cycle.
Most studies of soil enzymes have been confined to arable agricultural
and forest soils. But a flooded rice soil is predominantly anaerobic and as a
result differs from a nonflooded soil in several physical, chemical, and biologi-
cal characteristics. It has been reported that dehydrogenase/ETS activity is
higher in anaerobically or flooded incubated soil than aerobically incubated
soil (Orten and Neuhaus 1970). One of the important consequences of
flooding soil is a marked shift in favor of anaerobic microorganisms, the
increased ETS activity was related to the increase in the population of
anaerobic microorganisms in flooded soils as most dehydrogenases are of
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anaerobic origin (Orten and Neuhaus 1970). Tate (1979) observed a signifi-
cant increase in the dehydrogenase activity of soil under anaerobic conditions
though no change in the microbial numbers was detected. This, he suggested,
might be due to an increased role for the facultative and anaerobic bacteria. A
positive correlation was also observed between dehydrogenase activity and
soil moisture, and it was concluded that moisture was generally limiting to
the microbial activity (Tate and Terry 1980). Comparatively higher ETS
values in Crop I than in Crop II were observed particularly at the maturity
stage. It might be due to higher temperature at the time of sampling in Crop
I as soil sampling for Crop I was done in mid-July, while for Crop II, the
same stage was done in late October. Trevors observed that an increase in
temperature from 10 to 208C and from 20 to 308C caused increases in dehy-
drogenase activity by factors of 3.2 and 3.9, respectively (Trevors 1984). So,
the results are in full agreement with the previous findings. In the present
study, a consistent increase in the ETS activity was also observed, like
previous studies, during the different growth stages of rice as the rice crop
remained under anoxic (reduced) condition throughout its life cycle. Fluctu-
ations in the activity in some treatments/growth stages may be attributed to
the changes in the moisture, temperature, and inputs (fertilizers, pesticides),
as these conditions were changed from time to time during the study period.
In the field, of course, some conditions are beyond the control, specifically,
the main difference was the standing rice crop, which had influenced the
soil environment. In the planted soil, continuous addition of enzymes could
be expected from plant roots and associated microorganisms (Speir et al.
1980).
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