Ecological Indicators 132 (2021) 108262

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original Articles

Enhancing soil ecosystem services through sustainable integrated nutrient

management in double rice-cropping system of North-East India
Bhabesh Gogoi a, *, Nilay Borah b, Ajit Baishya c, Dhruba Jyoti Nath b, Samiron Dutta b,
Ranjan Das d, Debojit Bhattacharyya b, Karuna Kanta Sharma a, Donatella Valente e, *,
Irene Petrosillo e
a
Advanced Centre for Integrated Farming Systems Research, (AICRP on IFS under ICAR-IIFSR), Assam Agricultural University, Jorhat, Assam 785013, India
b
Department of Soil Science, Assam Agricultural University, Jorhat, Assam 785013, India
c
Directorate of Post Graduate Studies, Assam Agricultural University, Jorhat, Assam 785013, India
d
Department of Crop Physiology, Assam Agricultural University, Jorhat, Assam 785013, India
e
Department of Biological and Environmental Sciences and Technologies, University of Salento, Provle Lecce-Monteroni, 73100 Lecce, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: The wetland cultivation of rice is subjected to anaerobic and aerobic soil conditions causing substantial changes
Integrated nutrient management in the soil system. However, how long-term supplementation of organics with reduced chemical fertilizers affects
Enzymatic activity microbial composition, their activities, and enzymatic activities in acid soil has not been sufficiently investigated.
Microbial activity
This research is focused on a rice-rice system after an ongoing field experiment set-up in 1977–78 at Assam
Long-term monitoring
Soil ecosystem services
Agricultural University, Jorhat, India, where 7 alternative nutrient management have been investigated to: (1)
Rice-rice sequence assess the effects on soil organic carbon (SOC), microbial biomass carbon, and enzymatic activity in acid soil; (2)
identify and discuss the most suitable treatment combinations of organic and chemical fertilizers to enhance soil
ecosystem services (SES). Accordingly, we analysed the soil microbiological properties as affected by the 32 years
of continuous integrated nutrient management (INM) practices and also evaluated the INM treatments in terms of
SES. Results revealed that the soil microbial biomass carbon significantly varied across the treatments from 129.4
to 412.1 µg g− 1 which comprises 2.4 to 4.4% of the SOC. The highest bacterial count (8.95 log cfu g− 1 soil) was
recorded in RDF + Azolla treatment, whereas fungal count was the maximum (7.47 log cfu g− 1 soil) in RDF +
FYM treatment. All the enzymatic activities responded significantly to the INM practices, but the trend of
response was different for different enzymes. The highest dehydrogenase (223.6 µg TTF g− 1 soil 24 h− 1) and
urease (4.1 μg NH4-N g− 1 soil 2 h− 1) activities were recorded in RDF + Azolla, while phosphomonoeaterase
(337.4 μg p-nitrophenol g− 1 soil h− 1) and fluorescein diacetate hydrolysis (10.0 μg fluorescein g− 1 soil h− 1)
activities were found to be the maximum in RDF + FYM. The microbial and enzymatic activities decreased
significantly in the control after 32 cycles of rice-rice cropping. In this study, a significant positive statistical
correlation of all the microbiological properties with soil pH, soil organic carbon and grain yield of crops were
recorded. Finally, the different soil properties under the different nutrient treatments have been discussed in
terms of SES provision, highlighting that the most sustainable treatments have resulted in RDF + FYM, RDF + RS
and RDF + Azolla.

1. Introduction like lowering soil organic carbon (SOC), increasing soil acidification and
poor physical properties (Celik et al., 2010; Liu et al., 2010a), as it has
Intensive agriculture can guarantee food security worldwide, but at been observed in several long-term experiments (Nambiar, 1994), while
the cost of detrimental effects on soil health (Palm et al., 2014). Long- the integration of organic sources sustain the productivity (Liang et al.,
term application of nitrogenous fertilizers may cause several problems 2011; Nayak et al., 2012; Baishya et al., 2015). Although organic and

* Corresponding authors at: Department of Biological and Environmental Sciences and Technologies, University of Salento, Prov.le Lecce-Monteroni, 73100 Lecce,
Italy (D. Valente). Advanced Centre for Integrated Farming Systems Research, (AICRP on IFS under ICAR-IIFSR), Assam Agricultural University, Jorhat, Assam-785
013, India (B. Gogoi).
E-mail addresses: [email protected], [email protected] (B. Gogoi), [email protected] (D. Valente).

https://doi.org/10.1016/j.ecolind.2021.108262
Received 10 July 2021; Received in revised form 16 September 2021; Accepted 30 September 2021
Available online 5 October 2021
1470-160X/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
B. Gogoi et al. Ecological Indicators 132 (2021) 108262

inorganic fertilizers are used primarily to increase nutrient availability programme improves soil ecosystem services enhancing the productivity
to plants, they can affect the population, composition, and function of of rice-based cropping systems in the eastern Himalayan region of India
soil microorganisms (Marschner et al., 2003). The Integrated Nutrient as well as all over the world (Baishya et al., 2017; Babu et al., 2020).
Management (INM) practices have often been recommended for sus­ Long-term experiments from India (Nayak et al., 2012; Baishya et al.,
taining soil fertility and soil health (Baruah and Baruah, 2015) but also 2015; Yadav et al., 2017) and China (Liang et al., 2011; Tong et al.,
increase agronomic efficiency (Wu et al., 2020), for which it has been 2014) thoroughly confirmed that the nutrient integrations through
proposed as an alternative efficient practice for sustainable crop pro­ organic and inorganic sources of nutrients can progressively improve the
duction (Navarro-Noya et al., 2013; Zhang et al., 2018) original carbon levels and sustainability of rice-based cropping systems.
Soil ecosystem services (SES) are strongly affected by land-use The rice-rice sequence is the dominant cropping system providing
practices (Petrosillo et al., 2019), SOC, soil microbial biomass carbon livelihoods to millions of farmers in the eastern and north-eastern region
(SMBC), and soil enzymatic activity (Williams and Hedlund, 2013; of India (Baishya et al., 2016; Yadav et al., 2019). The wetland culti­
Jackson et al., 2019). In this context, SOC stock represents the support of vation of rice gives rise to anaerobic and aerobic soil conditions (during
many SES like nutrient cycling, water regulation, and climate regula­ crop and non-crop season, respectively) (Dong et al., 2014) causing
tion, but it can be depleted by land use management practices (Villarino substantial changes in microbial composition, their activities (Ge et al.,
et al., 2019) with effects on soil quality (Chen et al., 2021). It is 2008), and enzymatic activities (Nath et al., 2011). To better understand
important because of the fact that soils supply a wide range of ecosystem how rice cultivation can affect the functionality of soil, and then the
services (Costanza et al., 1997) crucial for human well-being and sus­ provision of SES, long-term experiments can play an important role
tainable quality of life (Ellili-Bargaoui et al., 2021). However, little because they can highlight the complex interaction among plants, soils,
attention has been given to land use impacts on SES (Blanco et al., 2018; climate, and management practices and their effects on crop produc­
Othoniel et al., 2016). tivity. The response of these soil microbial variables to inorganic and
Farmyard manure (FYM), crop stubbles, and Azolla represent organic amendments is often studied in the long-term experiments as a
important sources of organic matter in rice crops managed under inte­ marker of the soil status (Kussainova et al., 2013; Prakash et al., 2018) to
grated nutrient management (INM) systems (Baishya et al. 2015) and enhance the resilience of SES, since they can anticipate changes in soil
are likely to maintain C level sustaining the soil health under long-term quality before they are detected by other soil analyses (Ndiaye et al.,
(Mandal et al., 2007; Benbi and Senapati, 2010). For assessing the effects 2000). Such long-term experiments are the primary source of informa­
of agricultural practices on soil quality, the microbial community has tion to determine the effect of nutrient management in cropping systems
been considered as an important indicator because a shifting in their and thus, site-specific information is needed for evaluation of soil
community structures is coupled with changes in soil quality (Navarro- quality. Yet, concerning changes in biological properties as affected by
Noya et al., 2013; Sun et al., 2015). Although the soil quality depends on integrated supply of nutrients in acid soil under long-term double rice-
several soil parameters, biological processes are the most sensitive and cropping sequence of north-eastern region of India is relatively little
significant (Dick, 1992; De Paul Obade and Lal, 2016; Drobnik et al., known. Hence, this study was carried out in a rice-rice system under 32
2018). The role of soil organisms is crucial, because they are responsible years of INM practices to: (1) assess the effects of different treatment
of organic matter decomposition, nutrient cycling, soil fertility and combinations of supplementation of organic sources (farmyard manure/
quality for which maintaining high levels of microbial diversity in soil is rice stubbles/ Azolla) with reduced chemical fertilizers on SOC, SMBC,
the key for sustainable agriculture (Bastida et al., 2012; Preethi et al., and enzymatic activity in acid soil; (2) identify and discuss the most
2013; Sun et al., 2015; Bünemannet al., 2018). suitable treatment combinations of organic and chemical fertilizers to
The functional potentialities of microorganisms are indicated by the enhance soil ecosystem services (SES) in the prevailing climatic condi­
soil microbial biomass and enzymatic activities in soil. Estimation of tion of north-east India.
SMBC is considered as the most sensitive and important biological in­
dicator for assessing both short as well as long-term changes in soil 2. Materials and methods
fertility and quality (Powlson et al., 1987; Ladd et al., 1994; Bakh­
shandeh et al., 2019), although it comprises only 1–5% of the total 2.1. Study area
organic carbon (Jenkinson and Ladd, 1981; Smith and Paul, 1990; Malik
et al., 2018). Soil enzymes are important for their intimate relationship The long-term experiment was initiated during 1987–1988 at
to soil microbial activities (Ramirez et al., 2012), which directly affect Instructional-cum-Research Farm of Assam Agricultural University
soil stability and fertility, and are strongly involved in the dynamics of (AAU), Jorhat, Assam, India (26o48′ N, 95◦ 50′ E and altitude 86.6 m msl),
soil nutrient transformations (Frankenberger and Dick, 1983) and soil in which the current study has been carried out for 3 years from 2017–18
quality (Visser and Parkinson, 1992; Dick, 1994). Dehydrogenase (DHD) to 2019–20. The study area is flat (<2% slope) and the soil is sandy clay
is often most studied enzyme because of its occurrence in every viable loam in texture (sand 46.6%, silt 19.9%, and clay 33.5%). At the
microbial cell that determines the total oxidative potential of soil mi­ beginning of the experiment (1987–1988), the soil was tested acidic in
crobial community (Dick, 1997) reflecting the overall microbiological reaction (pH 5.0, EC 0.13 dS m− 1) with bulk density of 1.4 Mg m− 3,
activity in soil. Fluorescein di-acetate (FDA) provides comprehensive organic carbon of 6 g kg− 1, available N of 270 kg ha− 1, available P of 10
microbial activity in soils (Bendick and Dick, 1999). Further, a group of kg ha− 1 and available K of 147 kg ha− 1. The climate of the study area
enzymes called phosphomonoesterase (PMEase) catalyses the hydrolysis comes under humid subtropical with average annual rainfall of 1,900
of esters of phosphoric acid to release phosphate is of paramount mm, most of which received during July-October. The mean minimum
importance as a soil quality indicator (Trasar-Cepeda et al., 2008). Be­ and maximum annual temperature is observed in January (18.5 ± 1 ◦ C)
sides, the urease activity is widely used to assess the impact of soil and August (28.5 ± 1 ◦ C), respectively (Fig. 1).
management practices on soil quality (Diaz-Marcote et al., 1995).
Rice (Oryza sativa L.) is one of the most important food crop and a 2.2. Experimental design
primary food source for more than one third of world’s population
(Baishya et al., 2015). For meeting the needs of South-East Asia alone, The field experiment with 8 treatments (replicating thrice with in­
rice production must be enhanced up to 275 million tonnes by 2030 dividual plot sizes of 10 m × 10 m) was laid out in a randomized block
(Subbiah et al., 2001). However, several research witnessed the yield design. The treatments were composed of different combinations of
stagnation or declining yield trends in case of the double rice cropping organic and inorganic sources of nutrients to winter rice- autumn rice
systems without external sources of nutrients (Baishya et al., 2015). On cropping sequence and were applied for 32 years (Table 1).
the contrary, inclusion of organic inputs in fertility management To meet the 100% recommended N doses in the winter rice, the

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crop.
For the winter crop, a long duration (145–150 days) rice variety
Ranjit (30-days old seedlings) was transplanted at 20 cm × 20 cm
spacing in the last week of July and was harvested in the last week of
November. A medium duration (120–125 days) autumn rice variety
Disang (30-days old seedlings) was transplanted at 20 cm × 15 cm
spacing in the last week of March and was harvested in the last week of
June. The straw yield was reported at the harvest of the rice crops
whereas the grain yield of crops was reported at 14% grain moisture
content. All other crop management practices followed the recommen­
dation for the agro-climatic zone.

2.3. Soil sampling and analysis

Composite soil samples were prepared by collecting the samples

from three randomly selected points of each replicated plot at the end of
the rice- rice sequence during 2017–18, 2018–19, and 2019–20.
Fig. 1. Average meteorological parameters during the crop growth period at Immediately after collection, the soil samples were brought to the lab­
ICR farm of Assam Agricultural University (AAU), Jorhat, Assam (26o48′ N, oratory and a part of the samples were stored in a refrigerator at 4◦ C
95◦ 50′ E and 86.6 mt above msl). The data are the average of 3 years from temperature until analysed for the biological properties. The remaining
2017–2018 to 2019–2020. Source: Department of Agrometeorology, AAU, parts of soil samples were processed for the determination of organic
Jorhat, India. carbon following wet digestion method (Walkley and Black, 1934) and
soil pH (in 1: 2.5 soil–water suspension) as described by Jackson (1973).
The basic initial soil physico-chemical properties were analyzed using
Table 1
the standard procedures following Jackson (1973) and Baruah and
Treatment combinations used in the study under the rice-rice sequence.
Borthakur (1997).
SN. Treatment Symbol The initial biological properties of the soil were analyzed using the
Winter rice (cv. Ranjit) Autumn rice (cv. serial dilution technique (Martin, 1950) for the counting of bacteria and
Disang) fungi by the spread plate technique on nutrient agar medium and
T1 No fertilizer, No manure Control Unfertilized Martin’s Rose Bengal agar medium, respectively. The microbial numbers
(control) -control were estimated as colony forming units per gram (cfu g− 1) of soil on dry
T2 RDF RDF RDF
weight basis and transformed to log cfu g− 1. Microbial biomass carbon
T3 50% RDF + 2.5 t ha− 1 FYM RDF RDF + FYM
T4 75% RDF + 1.25 t ha− 1 FYM 75% RDF 75% RDF + FYM
(MBC) of soil was determined by chloroform fumigation extraction
T5 50% RDF + 3.0 t ha− 1 RS RDF RDF + RS method (Jenkinson and Powlson, 1976) and expressed as μg g− 1 soil
T6 75% RDF + 1.5 t ha− 1 RS 75% RDF 75% RDF + RS following Vance et al. (1987). For determination of fluorescein diacetate
T7 50% RDF + 0.5 t ha− 1 Azolla RDF RDF + Azolla (FDA) hydrolysis activity, the soil was incubated with FDA at 25 ◦ C for 1
T8 75% RDF + 0.25 t ha− 1 75% RDF 75% RDF + Azolla
h which was followed by the extraction process using an organic solvent
Azolla
mixture (2:1 chloroform: methanol). The amount of fluorescein finally
RDF: recommended dose of fertilizers of N, P and K (45, 30 and 40 kg ha− 1, formed was determined colorimetrically and was reported as μg fluo­
respectively); FYM: farmyard manure; RS: rice stubble rescein g− 1 soil h− 1 (Adam and Duncan, 2001). The dehydrogenase
(DHD) activity was determined by the reduction of triphenyl tetrazolium
chemical fertilizers were applied in combination with farmyard manure chloride (TTC) to triphenyl formazan (TPF) and was expressed on dry
(FYM), rice stubbles, or Azolla. However, the autumn rice received only weight as μg TPF g− 1 soil 24 h− 1 (Casida et al., 1964). Following
N-P-K fertilizers without any organic sources of nutrients. The chemical Tabatabai and Bremner (1969), the phosphomonoesterase (PMEase)
fertilizers with the recommended dose of N-P-K (45–30-40 kg ha− 1, activities was determined colorimetrically using p-nitrophenyl phos­
respectively) were applied in the form of urea, single super phosphate phate, and expressed as μg p-nitrophenol g− 1 soil h− 1. The urease ac­
(SSP), and muriate of potash (MOP), respectively as per the recom­ tivity in soil was reported as μg of ammonia released per gram of soil per
mended package of practices of the region. The N content of the organic two hour (i.e. μg NH4-N g− 1 soil 2 h− 1) following the method as
sources (FYM 0.9%, rice stubbles 0.7%, and Azolla 4.5%) were analysed described by Fawcwtt and Scott (1960).
and applied accordingly for a particular treatment to meet the 100% N
requirement by the winter rice crop. FYM (2.5 and 1.25 t ha− 1) and rice 2.4. Soil ecosystem services
stubbles (approximately 15 cm sized, 3.0 and 1.5 t ha− 1) were manually
spread uniformly and incorporated during the field preparation, 15 days The different treatments have been compared in order to discrimi­
before transplanting of winter rice crop. Azolla (Azolla caroliniana) as nate which are the most suitable to guarantee the provision of soil
biofertilizer was inoculated (0.5 and 0.25 t ha− 1 on a fresh weight basis) ecosystem services (SES). A literature review has helped in identifying
for dual cropping with winter rice (which covered approximately the linkages among the parameters and SES, then a spider diagram has
6.7–7.7% and 3.4–3.9% of the standing water surface in case of T7 and been used to evaluate, as a first approximation, the differences among
T8, respectively at the time of introduction). Azolla was incorporated the integrated management treatments in terms of SES.
into the soil at approximately 70–77 and 36–40% coverage of the sur­
face water (47 DAT in T7 and T8, respectively). In particular, half of urea, 2.5. Statistical analyses
whole quantity of SSP, and MOP were applied as basal at the time of
final land preparation. The remaining amount of urea was top-dressed at The statistical analysis of variance (ANOVA) was performed
the time of maximum tillering and panicle-initiation stage of the rice following Gomez and Gomez (1984) to investigate whether the INM
crop. In the case of winter rice, the 1st top dressing was done 27 days treatments had a significant influence on soil properties and yield of the
after transplanting (DAT) and 2nd top dressing at 55 DAT. Similarly, rice-rice system. The SAS-9.3 (SAS Institute, Cary, North Carolina, USA
top-dressing of urea was carried out at 22 and 42 DAT in the autumn rice 2013) was used to measure the least significant difference (LSD)

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between the means and correlation matrix calculation. Pearson’s cor­ year periods of double rice-cropping over RDF and INM treatments
relation coefficients among the grain yield and soil properties were also (Table 2).
performed. Unless stated, the significance level referred to the results is
p < 0.05. 3.5. Soil microbial count

3. Results The soil bacterial count augmented significantly with the INM
treatments and the data ranged from 5.06 to 8.95 log cfu g− 1 soil
3.1. The yield of crops under rice-rice system (Table 3). The highest bacterial count was recorded in RDF + Azolla (T7)
followed by RDF + FYM (T3), whereas the unfertilized-control (T1) was
The application of recommended N-P-K, either through chemical registered with the lowest bacterial count. Application of RDF + Azolla
fertilizers or in combination with organic sources significantly increased (T7) showed 45.0% and 76.8% increase in bacterial count over RDF (T2)
the yield of crop over control (Table 2). The highest grain and straw and unfertilized control (T1), respectively. Fungal count significantly
yields of the winter and autumn rice were obtained by 75% RDF + RS varied among the INM treatments ranging between 3.57 log cfu g− 1 soil
(T6) followed by RDF + RS (T5) and RDF + FYM (T3). The grain yield of under unfertilized-control (T1) and 7.47 log cfu g− 1 soil under RDF +
winter and autumn rice (2.01 and 1.70 Mg ha− 1, respectively) declined FYM (T3) (Table 3). The highest 109.2% increase in fungal count was
significantly in control plots receiving no external sources of nutrients observed in RDF + FYM (T3) followed by 82.1% in RDF + Azolla (T7)
for 32 cycles of rice-rice sequence. Similar result was observed in the compared to unfertilized-control (T1).
straw yield of rice (Table 2).
3.6. Soil enzymatic activities
3.2. Soil pH
In this study, all the enzymatic activities responded significantly to
The soil pH was significantly affected by the integrated supply of the integrated application of organic and inorganic sources of nutrients,
nutrients in the rice-rice system and the data varied from 4.75 to 5.71 at but the trend of response was different for different enzymes (Table 3).
the end of the sequence (Table 2). Data revealed that the application of The results showed an increase in enzymatic activities by the application
chemical fertilizers partially substituted with organic sources of nutri­ of sole chemical fertilizers over control, and supplementation of or­
ents continuously for 32 years increased the soil pH by 0.71 to 0.96 units ganics (FYM/ rice stubbles/ Azolla) along with the chemical fertilizers
over the unfertilized-control. The highest soil pH was recorded in RDF + further increased soil enzymatic activity. The maximum 74.5, 69.7, and
2.5 t ha− 1 FYM (T3) (5.71) and 75% RDF + 1.25 t ha− 1 FYM (T4) (5.62), 60.9% increase in dehydrogenase (DH) activity was recorded due to
whereas the lowest value (4.75) was observed in unfertilized-control long-term application of RDF + Azolla (T7), RDF + FYM (T3), and RDF +
(T1) (Table 2). FYM (T5), respectively over the unfertilized-control (T1) (Table 3). The
phospho-monoesterase (PMEase) activity varied significantly between
3.3. Soil organic carbon 203.8 and 337.4 μg p-nitrophenol g− 1 soil h− 1 (Table 3). The highest
PMEase activity was recorded in RDF + FYM (T3), RDF + RS (T5), and
There was a significant change in soil organic carbon (SOC) over a RDF + Azolla (T7) compared to unfertilized-control (T1). Application of
32-year period of integrated nutrient management (INM) in the rice-rice RDF (T2) over 32-year periods enhanced the fluorescein diacetate (FDA)
system (Table 2). SOC ranged between 5.3 and 10.9 g kg− 1. Significantly hydrolysis in soil significantly by 32.3% over control (T1) (5.3 μg fluo­
higher SOC was recorded in RDF + RS (T5) and RDF + FYM (T3), fol­ rescein g− 1 soil h− 1). Significant increase in FDA hydrolysis
lowed by RDF + Azolla (T7) and 75% RDF + RS (T6). The plot that has (54.1–88.7%) due to INM treatments were also observed over
not received manures and fertilizers (T1) under the rice-rice system unfertilized-control (T1). The soil urease activity varied significantly
showed the lowest SOC. from 1.7 to 4.1 μg NH4-N g− 1 soil 2 h− 1 across the treatments under
study (Table 3). The maximum increase in urease activities was recorded
3.4. Soil microbial biomass carbon in RDF + Azolla (142.2%), RDF + FYM (116.5%), and RDF + RS (97.1%)
over the unfertilized-control. There was a decrease in activities of all the
The soil microbial biomass carbon (SMBC) content varied signifi­ enzymes in the unfertilized-control plot receiving no external sources of
cantly ranging from 129.4 µg g− 1 under unfertilized-control to 412.1 µg nutrients for 32 years of rice-rice cropping system compared to INM
g− 1 under RDF + Azolla (Table 2). The application of RDF + Azolla (T7) treatments.
enhanced the SMBC by 218.5% followed by 185.7% under RDF + FYM
(T3) over control (T1). The SMBC under different INM treatments 3.7. Pearson correlation analyses
significantly varied in the order T7 > T3 > T5 > T8 > T4 > T6 > T2 > T1
after 32-crop cycles of the rice-rice system. A remarkable decrease in Pearson correlation analyses (Table 4) showed that grain yield of
SMBC (10.4%) in the unfertilized-control plot was recorded after 32- winter and autumn rice was significantly and positively correlated with

Table 2
Effect of long-term integrated supply of nutrients on soil properties and yield of crops under rice-rice sequence.
Treatment* Soil pH (1:2.5) SOC (g kg− 1) SMBC (µg g− 1) Yield of winter rice cv. Ranjit (Mg ha− 1) Yield of autumn rice cv. Disang (Mg ha− 1)

Grain yield Straw yield Grain yield Straw yield

T1 4.75e 5.30e 129.4f 2.01d 2.90f 1.70d 2.70c

T2 4.95d 7.87 cd 258.8e 3.60c 4.64de 2.86bc 3.68ab
T3 5.71a 10.58a 369.7b 3.90abc 5.10bc 3.20a 3.88ab
T4 5.62ab 8.23c 304.2d 3.78bc 4.85 cd 3.03ab 3.68ab
T5 5.50c 10.87a 332.7c 4.04ab 5.32ab 3.23a 4.10a
T6 5.52bc 9.11b 297.5d 4.23a 5.60a 2.90bc 3.82ab
T7 5.50c 9.40b 412.1a 3.70bc 4.79 cd 3.10ab 3.70ab
T8 5.46c 7.64d 324.0c 3.55c 4.40e 2.63c 3.65b

SOC, Soil organic carbon; SMBC, Soil microbial biomass carbon;

*
Refer Table 1 for treatment details. Different lowercase letters in the same column indicate significant differences among treatments (p < 0.05).

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Table 3
Soil bacteria, fungi, and enzymatic activities and their contribution to soil ecosystem services (SES) as influenced by long-term integrated application of organic and
inorganic sources of nutrients in the rice-rice system(data given are the mean value of 3 years).
Treatments Bacteria (log Fungi (log Dehydrogenase (µg TTF Phospho-monoeaterase (μg p- Fluorescein di-acetate Urease (μg NH4- Support to
* cfu g− 1 soil) cfu g− 1 soil) g− 1 soil 24 h− 1) nitrophenol g− 1 soil h− 1) hydrolysis (μg fluorescein g− 1
N g− 1 soil 2 h− 1) SES
soil h− 1)

T1 5.06 h 3.57 g 128.1e 203.6f 5.3f 1.7e ↑

T2 6.17 g 4.30f 167.1d 265.1e 7.0e 2.9d ↑↑
T3 8.00b 7.47a 217.5ab 337.4a 10.0a 3.7b ↑↑↑
T4 7.05e 5.30d 185.0 cd 305.7bc 9.0c 3.3c ↑↑
T5 7.50c 5.57c 206.1abc 331.6a 9.2bc 3.5bc ↑↑↑
T6 6.97f 5.00e 181.9 cd 297.5 cd 8.2d 3.4c ↑↑
T7 8.95a 6.50b 223.6a 318.0ab 9.5b 4.1a ↑↑↑
T8 7.17d 5.37 cd 195.3bc 284.2de 9.0c 3.3c ↑↑
*
Refer to Table 1 for treatment details. Data within columns followed by different lowercase letters are significantly different (p < 0.05)

Table 4
Pearson correlation matrix for grain yield and different soil properties after 32-year application of different organic and inorganic sources of nutrients under rice-rice
system.
Parameters GYWR GYAR Soil pH SOC SMBC Bacteria Fungi DH PMEase FDA Urease

GYWR 1.00
GYAR 0.77* 1.00
Soil pH 0.79* 0.75* 1.00
SOC 0.87** 0.93** 0.77* 1.00
SMBC 0.88** 0.90** 0.79* 0.97** 1.00
Bacteria 0.84** 0.83** 0.88** 0.95** 0.92** 1.00
Fungi 0.79* 0.84** 0.70* 0.87** 0.93** 0.84** 1.00
DH 0.89** 0.95** 0.87** 0.93** 0.89** 0.90** 0.90** 1.00
PMEase 0.88** 0.85** 0.79* 0.83** 0.87** 0.92** 0.96** 0.91** 1.00
FDA 0.77* 0.79* 0.75* 0.89** 0.84** 0.77* 0.95** 0.79* 0.86** 1.00
Urease 0.91** 0.93** 0.78* 0.86** 0.85** 0.79* 0.92** 0.86** 0.95** 0.86** 1.00

GYWR, Grain yield of winter rice; GYAR, Grain yield of autumn rice; SOC, Soil organic carbon; SMBC, Soil microbial biomass carbon; DH, Dehydrogenase; PMEase,
Phosphomonoesterase; FDA, Fluorescein diacetate
*
significant at 5% level,
**
significant at 1% level

soil pH, SOC, SMBC, soil bacterial activity, and fungal activity. In the
present study, all the enzymatic activities viz., DH, PMEase, FDA, and
urease activity showed a significant positive relationship with the grain
yield of winter rice. Similar trend was observed in the case of autumn
rice crops. The positive and significant correlation of all the microbio­
logical properties with soil pH and SOC were also recorded (Table 4).

3.8. Soil ecosystem services

Healthy soil yields a sustainable flow of ecosystem services, like

nutrient cycling and climate regulation (Dominati et al., 2010), how­
ever, very often ecosystem services’ researches lack in data about soil
components (Liu et al., 2010b). Soil ecosystem services depend on soil
properties that are the basis for soil functionality, as highlighted in
Fig. 2, and they are affected by soil management practices (Adhikari and
Hartemink, 2016). In a recent review on soil ecosystem services, Adhi­
kari and Hartemink (2016) have highlighted that soil properties support
the performances of soil functions with effects on soil ecosystem services
such as carbon sequestration, nutrient cycling and capacity, food, soil
biodiversity, and primary production.
Fig. 2. Conceptual diagram linking sustainable integrated nutrient manage­
The comparison among the treatments, including the control, has ment to soil properties, functions, and ecosystem services.
noticed that sustainable INM can strongly affect soil properties such as
SOC, soil pH, and soil biota in terms of bacteria and fungi (Table 3). The
activity. Therefore, this gives management practices a crucial re­
integration of the results of this study throughout the spider diagram
sponsibility in enhancing ecosystem services. This research has
(Fig. 3) has allowed to underline the potential capacity to provide soil
attempted to indicate as a first approximation which integrated nutrient
ecosystem services under different treatments in an integrated nutrient
management could be more effective to foster the soil ecosystem ser­
management (INM) practice based on the use of organic manures and
vices in rice-rice cultivation.
chemical fertilizers with the aim to enhance soil fertility. The most
sustainable treatments have resulted in T3, T5 and T7, highlighted in
Fig. 3 and Table 3, because of higher levels in terms of the yield of crops,
soil microbial biomass carbon and microbial count, and enzymatic

5
B. Gogoi et al. Ecological Indicators 132 (2021) 108262

4.2. Soil microbial biomass carbon and soil microbial count

The soil microbial biomass carbon (SMBC) constitutes a small

portion (1–5%) of the SOC (Jenkinson and Ladd, 1981; Smith and Paul,
1990). However, it is the most sensitive one for assessing short-term
changes in soil fertility and quality (Powlson et al., 1987; Ladd et al.,
1994). In this study, the SMBC significantly varied with INM treatments
contributing 2.4–4.4% to the SOC (Fig. 4). These values fit within those
reported by Vance et al. (1987) for several terrestrial ecosystems
(61–1900 µg g− 1).
The application of organic input (FYM/ crop stubbles/ Azolla) is
normally associated with the increase in SMBC (Banerjee et al., 2006;
Kaur et al., 2008; Stockmann et al., 2013). In general, organic inputs
enhance the development of microflora that, ultimately, increases the
global activity of soil (Ros et al., 2003; Nath et al., 2012). Long-term
integrated supply of nutrients increased the SMBC content in two
ways: first, due to higher biomass production and their decomposition
with consequent steady nutrient release (chiefly C and N) (Lee et al.,
2009; Ge et al., 2017), and second, constant supply of readily metabo­
Fig. 3. Spider diagram showing the effect of integrated nutrient management lizable organic C and N to support microbial proliferation (Prakash et al.,
on soil properties including the soil biota. Refer to Table 1 for treatment details. 2016; Tripura et al., 2018; Tao et al., 2020). The maximum SMBC
SOC, Soil organic carbon; SMBC, Soil microbial biomass carbon; DH, Dehy­ recorded with the integrated application of RDF + Azolla was probably
drogenase; PMEase, Phosphomonoesterase; FDA, Fluorescein diacetate. due to the higher availability of substrate C, because the Azolla appli­
cation is known to produce diverse growth-promoting substances that
4. Discussion might contribute to the intense proliferation of microbial growth
(Bhuvaneshwari and Singh, 2012). The findings of Gogoi et al. (2010)
4.1. The yield of crops under rice-rice system supported such results as they reported the highest content of SMBC in
acid soil under biofertilizer-based INM package treatment, followed by
The present study clearly showed the significance of integrated the treatment of 50% RDF (chemical) + 50% N (FYM). Tripura et al.
application of organic sources (FYM/rice stubbles/Azolla) with inor­ (2018) reported that INM helps in increasing the root biomass and ex­
ganic fertilizers in increasing the yield of crop over control. Yield in­ udates, as highlighted in this study, due to better crop growth resulting
crease under INM treatments might be attributed to better soil health in higher SMBC. Furthermore, it is possible to suppose that soil of the
resulting from the increase in SOC (Baishya et al., 2015). Combined experimental site was C-limited, and the supplementation of FYM/ rice
application of organic and inorganic sources can control the release of stubbles/ Azolla has provided an organic input for microorganisms, with
nutrients in the soil through mineralization of organic substances that consequent improvement in SMBC (Verma and Mathur, 2009; Nayak
facilitated better crop growth (Acharya et al., 2012; Shahid et al., 2013). et al., 2012; Luo et al., 2015; Chen et al., 2017).
These findings are in-tune with earlier reports (Nayak et al., 2012; Yan Soil microorganisms are important to agro-ecosystems as they
et al., 2013). On the other side, the recorded significant declining trend perform key roles in various soil processes (Wu et al., 2011). Continuous
in the grain and straw yield in unfertilized-control was probably related fertilization with organic and inorganic sources alters the soil health and
to the decline of SOC and the associated reduction in nutrient supply capacity of soil to function as it changes in physico-chemical and bio­
(Nayak et al., 2012; Baishya et al., 2015). logical properties of soil directly or indirectly (Murugan and Kumar,
The significant variations in soil pH under the INM treatments over 2013). Therefore, in recent years, the microbial count has been used
unfertilized-control plot thus were confirmed by the results of ANOVA
(p < 0.05). The accumulation of organic acids from the root exudates as
well as continuous use of acid forming chemical fertilizers (like urea)
under long-term (32 years) could be the possible reasons for increase in
soil acidity in the unfertilized-control (T1) and RDF (T2) as highlighted
by Manna et al. (2013). On the contrary, the INM treatments showed an
increase in soil pH as noticed also by Sushma et al. (2007) and Baishya
et al. (2015).
The long-term chemical fertilization and INM treatments signifi­
cantly enhanced the SOC compared to unfertilized-plot (Zhang et al.,
2018; Tao et al., 2020). The increased SOC by chemical fertilization may
be due to the fact of better crop growth resulting in addition of greater
amount of residual biomass in soil through root, leaves, stubble and
rhizodeposition. Similar findings were reported by previous workers
(Kundu et al., 2007; Singh et al., 2012; Ramdas et al., 2017). Constant
supplementation of organic sources of nutrients (FYM/ rice stubbles/
Azolla) along with chemical fertilizers stimulated the growth and ac­
tivity of microorganisms (Table 3) besides increasing root and other
biomass in soil which ultimately enhanced SOC noticeably after 32 crop
cycles of rice-rice sequence as highlighted by Zhang et al. (2010) and
Thakur et al. (2011). Fig. 4. Percent contribution of soil microbial biomass carbon (SMBC) to soil
organic carbon (SOC) content in acid soil under rice-rice system. Refer to
Table 1 for treatment details. The columns (average of 3 years) followed by a
common letter in the parameter are not differ significantly at p < 0.05.

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B. Gogoi et al. Ecological Indicators 132 (2021) 108262

widely to describe the soil quality under different agricultural practices. amended, soil is related to increase in the population of microorganisms
The studies on the responses of soil microbial diversity to integrated with increased availability of substrate through production of diverse
supply of nutrients reported an increase in soil microbial diversity extracellular enzymes (Sheoran et al., 2020). Besides, the root exudates
(Wang et al. 2014), while other studies showed no significant changes of the rice crop promoted the production of nitrogenous substances
(Sun et al., 2015), and even a decrease in microbial diversity (Banerjee which probably induced the urease activity (Elayearja and Singravel,
et al. 2016). From our study, it was evident that only chemical fertil­ 2011; Ramdas et al., 2017).
izations (T2) in the rice-rice system over 32-year periods increased the
bacterial and fungal count as compared to unfertilized soil (T1). Singh 4.4. Soil ecosystem services
et al. (2012) reported an increase in productivity and incorporation of
larger residual biomass through root, leaves, and rhizodeposition due to Soil quality is determined by a suite of factors such as climate con­
chemical fertilization. Chu et al. (2007) reported a little effect of long- ditions, plant cover, edaphic biota, and their changes due to human land
term fertilization on the richness and diversity of soil bacterial and use and management (Rinot et al., 2019). Differently from natural
fungal communities expect for organic matter-fertilized treatments. The ecosystems, croplands are affected by farming management practices,
addition of FYM/ rice stubbles/ Azolla with chemical fertilizers (i.e., T3, impacting on the provision of ecosystem services. Agricultural fertil­
T5 and T7) showed further increases in microbial count over unfertilized- ization is an example of farming practice essential to improve crop
control (T1) and RDF (T2), as demonstrated also by Nair and Ngouajio productivity worldwide, however the most recent literature has pro­
(2012), Navarro-Noya et al. (2013), and Tao et al. (2020). The INM vided evidence that organic fertilizer amendments play vital roles in
treatments might have provided more labile C substances needed for improving cropland fertility and productivity maintaining soil
maintenance of a larger population of soil bacteria and fungi (Prakash ecosystem services (Chen et al., 2019; Ferrarini et al., 2018). The
et al., 2016). Azolla being a biofertilizer increased the bacterial popu­ treatments T1 (unfertilized-control) and T2 (RDF) are the least per­
lation in soil which might be the possible reason for counting maximum forming in terms of soil properties’ maintenance and, therefore, in the
bacterial colonies in T7 receiving 0.5 t ha− 1 Azolla with reduced chem­ provision of soil ecosystem services, while T3, T5, and T7 are the best
ical fertilizers in the rice-rice system. performing and are all characterized by 50% RDF integrated with
farmyard manure, rice stubble, and Azolla, respectively.
4.3. Enzymatic activity Research on the linkages between the conversion of land-use classes
and the provision of services are useful to determine where the hot-spots
Soil enzyme activities are sensitive to organic amendments (Bohme of landscape service’ provision are located (Marinelli et al., 2021), while
et al., 2005; Zhao et al., 2016). Long-term application of organic inputs research linking the different management practices with the provision
increases the microbial and enzymatic activities in soil (Preethi et al., of soil ecosystem services can help in identifying the most sustainable
2013; Chang et al., 2014). The dehydrogenase (DH) enzyme, due to its agricultural practices able to enhance soil integrity, functionality, and
occurrence in every viable microbial cell, determines the overall soil resilience. The focus on soil ecosystem services integrates the traditional
microbiological activity (Nannipieri et al., 2011). DH activities in soil agricultural performance assessment, based mainly on the agro-
depend mostly on SOC and N content in soil and are greatly influenced economic perspective (agricultural production and income), with
by long-term fertilization (Katkar et al., 2011; Patel et al., 2018), as ecological evaluations. In this sense, the ability to maintain desired
highlighted by the present study: +74.5% in T7 and + 69.7% in T3 over levels of agricultural productivity in a changing world derives from the
control (T1) and that represent a real-time indication of better soil health capacity to guarantee the provision of soil ecosystem services and, thus,
after 32 cycles of rice-rice system. Previous workers also reported the robustness of such crop systems in terms of resilience.
increased DH activity by INM treatments (Ramdas et al., 2017; Mandal
et al., 2018). 5. Conclusions
The PMEase activity in soil under the rice-rice system varied in the
order FYM > rice stubbles > Azolla in accordance with the results of This research has explored the complexity behind different inte­
other studies (Nath et al., 2012; Biswas and Narayanasamy, 2006). The grated nutrient management of rice-rice cultivation choices, through a
significantly greater activity of PMEase in the organic (FYM/ rice long term monitoring program, by combining a multiple set of indicators
stubbles/ Azolla) amended plots could be attributed to enhanced mi­ for each real management scenario. Thirty two years of rice-rice culti­
crobial activity and the concomitant release of more organically bound P vation with the supplementation of organics (FYM/ rice stubbles/
in the soil, as reported also by Mandal et al. (2007), recognizing the Azolla) partially substituting the recommended quantities of fertilizers
significant influence of soil pH on the activity of PMEase in soil (Dick, significantly enhanced the microbial and enzymatic activities with the
1994). contribution to build-up of organic carbon and microbial biomass car­
One of the most appropriate indicators for monitoring the effects of bon in acid soil. Long-term integrated supply of nutrients was able to
different soil management practices on soil biology is fluorescein diac­ influence soil pH favourably increasing the yield of the crops. Supple­
etate (FDA). In the present study, the INM treatments analyzed in rice- mentation of 0.5 t ha− 1 Azolla + 50% recommended dose of fertilizers
rice system showed an increase from + 54.1% to 88.5% of FDA activ­ (RDF) in winter rice following 100% RDF in autumn rice (T7) showed
ity over control. The continuous supplementations of biomaterials the highest bacterial count in the soil, whereas fungal count was
(FYM/ rice stubbles/ Azolla) along with the chemical fertilizers maximum in case of the plot receiving 2.5 t ha− 1 farmyard manure +
enhanced the SOC content that might have increased the activities of 50% RDF in winter rice following 100% RDF in autumn rice (T3). We
proteases, lipases, and esterases in the soil (Nath et al., 2012; Nayak recorded the highest dehydrogenase and urease activities in T7, while
et al., 2007). The FDA is hydrolyzed by these enzymes in soil providing a phosphomonoeaterase and fluorescein diacetate hydrolysis activities
comprehensive microbial activity (Nath et al., 2011). were the maximum in T3. Hence, it was evident that the application of
The urease activity is affected profoundly by the nutrient manage­ organic inputs with reduced doses of chemical fertilizers is highly potent
ment practices involving both organic and inorganic sources (Diaz- to augment microbial and enzymatic activities in soil. Our study also
Marcote et al., 1995). In this research, 2.4, 2.2 and 2.0 times increase in showed that a double rice-cropping system without external sources of
urease activity were recorded in RDF + Azolla (T7), RDF + FYM (T3), and nutrients severely affected the yield, soil pH, organic carbon, and
RDF + rice stubbles (T5), respectively over unfertilized-control (T1) after microbiological properties after 32 cycles of cropping. The bacterial and
32 cycles of rice-rice cropping. Higher concentration of N stimulates the fungal count and enzymatic activities decrease significantly in the
urease activity in soil amended with different C substrates (Shukla and unfertilized-control as compared to the recommended dose of fertilizers
Varma, 2011), since the enhancement in urease activity in manure and integrated nutrient management practices under long-term. Finally,

7
B. Gogoi et al. Ecological Indicators 132 (2021) 108262

an integrated nutrient management with organic (FYM/ rice stubbles/ Banerjee, S., Kirkby, C.A., Schmutter, D., Bissett, A., Kirkegaard, J.A., Richardson, A.E.,
2016. Network analysis reveals functional redundancy and keystone taxa amongst
Azolla) and inorganic sources is absolutely indispensable not only to
bacterial and fungal communities during organic matter decomposition in an arable
sustain the productivity of rice-rice system but also to maintain soil soil. Soil Biol. Biochem. 97, 188–198.
health and soil ecosystem services. It is also recommended for further Baruah, A., Baruah, K.K., 2015. Organic manures and crop residues as fertilizer
study to address the issue of soil health and ecosystem services under substitutes: impact on nitrous oxide emission, plant growth and grain yield in pre-
monsoon rice cropping system. J. Environ. Prot. 06 (07), 755–770. https://doi.org/
various long-term management practices, for different soil types and 10.4236/jep.2015.67069.
agricultural systems under the prevailing climatic condition of North- Baruah, T.C., Borthakur, H.P., 1997. A Textbook of Soil Analysis. Vikas Publ. House Pvt.
East India which is considered as the key knowledge gap in this region. Ltd., New Delhi.
Bastida, F., Jindo, K., Moreno, J.L., Hernandez, T., Garcia, C., 2012. Effect of organic
Sustainable agricultural practices based on organic supply can be amendments on soil carbon fractions, enzyme activity and humus- enzyme
utilized for improving food production by reducing the environmental complexes under semi-arid conditions. Eur. J. Soil Biol. 53, 94–102.
risks related to the loss of soil ecosystem services caused by chemical Benbi, D.K., Senapati, N., 2010. Soil aggregation and carbon and nitrogen stabilization in
relation to residue and manure application in rice-wheat systems in northwest India.
amendments. In line with the 2030 Agenda for Sustainable Develop­ Nutr. Cycl. Agroecosys. 87 (2), 233–247.
ment, aiming at sustaining natural resources, food and agriculture, Bendick, A.K., Dick, R.P., 1999. Field management effects on soil enzyme activities. Soil
future research are still needed in order to enhance sustainable land-use Biol. Biochem. 31, 1471–1479.
Bhuvaneshwari, K., Singh, P.K., 2012. Organic rice production using organic manures
and organic rice farming based on local stakeholders’ knowledge of the and bio inoculants in alkaline soil. J. Recent Adv. Agric. 1 (4), 128–134.
contribution of soils to ecosystem services. Biswas, D.R., Narayanasamy, G., 2006. Rock phosphate enriched compost: an approach
to improve low grade Indian rock phosphate. Biores. Tech. 97, 2243–2251.
Blanco, C.F., Marques, A., van Bodegom, P.M., 2018. An integrated framework to assess
CRediT authorship contribution statement impacts on ecosystem services in LCA demonstrated by a case study of mining in
Chile. Ecosyst. Serv. 30, 211–219.
Bhabesh Gogoi: Investigation, Methodology, Data curation, Vali­ Bohme, L., Langer, U., Bohme, F., 2005. Microbial biomass, enzyme activities and
microbial community structure in two European long-term field experiments. Agr.
dation, Writing – review & editing. Nilay Borah: Supervision. Ajit Ecosyst. Environ. 109, 141–152.
Baishya: Conceptualization, Funding acquisition. Dhruba Jyoti Nath: Bünemann, E.K., Bongiorno, G., Bai, Z., Creamer, R.E., De Deyn, G., de Goede, R.,
Resources. Samiron Dutta: Formal analysis. Ranjan Das: Resources. Fleskens, L., Geissen, V., Kuyper, T.W., Mäder, P., Pulleman, M., Sukkel, W., van
Groenigen, J.W., Brussaard, L., 2018. Soil quality- a critical review. Soil Biol.
Debojit Bhattacharyya: Resources. Karuna Kanta Sharma: Project Biochem. 120, 105–125.
administration. Donatella Valente: Writing – review & editing. Irene Casida, L.E., Klein, D.A., Santoro, R., 1964. Soil dehydrogenase activity. Soil Sci. 98,
Petrosillo: Writing – review & editing, Supervision. 371–376.
Celik, I., Gunal, H., Budak, M., Akpinar, C., 2010. Effects of long-term organic and
mineral fertilizers on bulk density and penetration resistance in semi-arid
Mediterranean soil conditions. Geoderma 160 (2), 236–243.
Declaration of Competing Interest Chang, E., Wang, C., Chen, C., Chung, R., 2014. Effects of long-term treatments of
different organic fertilizers complemented with chemical N fertilizer on the chemical
and biological properties of soils. Soil Sci. Plant Nutr. 60, 499–511.
The authors declare that they have no known competing financial Chen, H.-P., Lee, M., Chiueh, P.-T., 2021. Creating ecosystem services assessment models
interests or personal relationships that could have appeared to influence incorporating land use impacts based on soil quality. Sci. Total Environ. 773,
the work reported in this paper. 145018. https://doi.org/10.1016/j.scitotenv.2021.145018.
Chen, L., Redmile-Gordon, M., Li, J., Zhang, J., Xin, X., Zhang, C., Ma, D., Zhou, Y., 2019.
Linking cropland ecosystem services to microbiome taxonomic composition and
Acknowledgements functional composition in a sandy loam soil with 28-year organic and inorganic
fertilizer regimes. Appl. Soil Ecol. 139, 1–9.
Chen, D., Yuan, L., Liu, Y., Jib, J., Hou, H., 2017. Long-term application of manures plus
This research has been funded by the Indian Council of Agricultural chemical fertilizers sustained high rice yield and improved soil chemical and
Research-Indian Institute of Farming Systems Research (ICAR-IIFSR), bacterial properties. Eur. J. Agron. 90, 34–42.
Meerut, India. Chu, H., Lin, X., Fujii, T., Morimoto, S., Yagi, K., Hu, J., Zhang, J., 2007. Soil microbial
biomass, dehydrogenase activity, bacterial community structure in response to long-
term fertilizer management. Soil Biol. Biochem. 39, 2971–2976.
References Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K.,
Naeem, S., O’Neill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., van den Belt, M., 1997.
The value of the world’s ecosystem services and natural capital. Nature 387 (6630),
Acharya, C.N., Dash, A.K., Senapati, H.K., 2012. Effect of integrated nutrient
253–260. https://doi.org/10.1038/387253a0.
management on microbial activity influencing grain yield under rice-rice cropping
De Paul Obade, V., Lal, R., 2016. A standardized soil quality index for diverse field
system in an acid soil. Asian J. Microb. Biotech. Environ. Sci. 14, 365–368.
conditions. Sci. Total Environ. 541, 424–434.
Adam, G., Duncan, H., 2001. Development of a sensitive and rapid method for the
Diaz-Marcote, I., Polo, A., Ceccanti, B., 1995. Enzymatic activities in a soil amended with
measurement of total microbial activity using fluorescein diacetate in a range of
organic wastes at semiarid field conditions. Arid Soil Res. Rehabil. 9, 317–325.
soils. Soil Biol. Biochem. 33, 943–951.
Dick, R.P., 1992. A review: long-term effects of agricultural systems on soil biochemical
Adhikari, K., Hartemink, A.E., 2016. Linking soils to ecosystem services — a global
and microbial parameters. Agric. Ecosyst. Environ. 40, 25–36.
review. Geoderma 262, 101–111. https://doi.org/10.1016/j.
Dick, R.P., 1997. Soil enzyme activities as integrative indicators of soil health. In:
geoderma.2015.08.009.
Pankhurst, C.E., Doube, B.M., Gupta, V.V.S.R. (Eds.), Biological indicators of soil
Babu, S., Singh, R., Avasthe, R.K., Yadav, G.S., Mohapatra, K.P., Selvan, T., Das, A.,
health. CABI, Wallingford, Oxfordshire, pp. 121–156.
Singh, V.K., Valente, D., Petrosillo, I., 2020. Soil carbon dynamics in Indian
Dick, R.P. 1994. Soil enzyme activities as indicators of soil quality. In: Doran, J.W.,
Himalayan intensified organic rice-based cropping sequences. Ecol. Indic. 114,
Coleman, D.C., Bezdicek, D.F., Stewart, B.A. (Eds.), defining soil quality for a
106292. https://doi.org/10.1016/j.ecolind.2020.106292.
sustainable environment. SSSA special publication no 35, ASA and SSSA, Madison,
Baishya, A., Gogoi, B., Hazarika, J., Borah, M., Hazarika, J.P., Bora, A.S., Rajbongshi, A.,
WI, pp. 104-124.
Deori, P., Sutradhar, P., 2015. Effect of continuous cropping and integrated nutrient
Dominati, E., Patterson, M., Mackay, A., 2010. A framework for classifying and
management practices on soil properties and yield of rice-rice cropping system in
quantifying the natural capital and ecosystem services of soils. Ecol. Econ. 69 (9),
acid soil. Ind. J. Agron. 60, 493–501.
1858–1868. https://doi.org/10.1016/j.ecolecon.2010.05.002.
Baishya, A., Gogoi, B., Hazarika, J., Hazarika, J.P., Bora, A.S., Das, A.K., Borah, M.,
Dong, W.Y., Zhang, X.Y., Dai, X.Q., Fu, X.L., Yang, F.T., Liu, X.Y., Sun, X.M., Wen, X.F.,
Sutradhar, P., 2016. Maximizing soil productivity and profitability through crop
Schaeffer, S., 2014. Changes in soil microbial community composition in response to
intensification and diversification with rice (Oryza sativa)-based cropping systems in
fertilization of paddy soils in subtropical China. Appl. Soil Ecol. 84, 140–147.
acid soils of Assam. Ind. J. Agron. 61, 274–280.
Drobnik, T., Greiner, L., Keller, A., Grêt-Regamey, A., 2018. Soil quality indicators – from
Baishya, A., Gogoi, B., Hazarika, J., Hazarika, J.P., Bora, A.S., Das, A.K., Borah, M.,
soil functions to ecosystem services. Ecol. Indic. 94, 151–169.
Sutradhar, P., 2017. Comparative assessment of organic, inorganic and integrated
Elayearja, D., Singravel, R., 2011. Influence of organics and various levels of NPK on soil
management practices in rice (Oryza sativa)-based cropping system in acid soil of
nutrient availability, enzyme activity and yield of groundnut in coastal sandy soils.
Assam. Ind. J. Agron. 62, 118–126.
J. Ind. Soc. Soil Sci. 59, 300–303.
Bakhshandeh, E., Hossieni, M., Zeraatpisheh, M., Francaviglia, R., 2019. Land use change
Ellili-Bargaoui, Y., Walter, C., Lemercier, B., Michot, D., 2021. Assessment of six soil
effects on soil quality and biological fertility: a case study in northern Iran. Eur. J.
ecosystem services by coupling simulation modelling and field measurement of soil
Soil Biol. 95, 103119. https://doi.org/10.1016/j.ejsobi.2019.103119.
properties. Ecol. Indic. 121, 107211.
Banerjee, B., Aggarwal, P.K., Pathak, H., Singh, A.K., Chaudhury, A., 2006. Dynamics of
Fawcwtt, J.K., Scott, J.E., 1960. A rapid and precise method for the determination of
organic carbon and microbial biomass in alluvial soil with tillage and amendments in
urea. J. Clin. Pathol. 13, 156–159.
rice–wheat systems. Environ. Monit. Assess. 119, 173–189.

8
B. Gogoi et al. Ecological Indicators 132 (2021) 108262

Ferrarini, A., Bini, C., Amaducci, S., 2018. Soil and ecosystem services: current Nambiar, K.K.M., 1994. Soil Fertility and Crop Productivity Under Long-Term Fertilizer
knowledge and evidences from Italian case studies. Appl. Soil Ecol. 123, 693–698. Use in India. Indian Council for Agricultural Research, New Delhi, India.
Frankenberger, W.T., Dick, W.A., 1983. Relationships between enzyme activities and Nannipieri, P., Giagnoni, L., Landi, L., Renella, G., 2011. Role of phosphatase enzymes in
microbial growth and activity indices in soil. Soil Sci. Soc. Am J. 47, 945–951. soil. In: Phosphorous in Action, 26th Edn. Springer, Berlin, pp. 215–243.
Ge, T., Li, B., Zhu, Z., Hu, Y., Yuan, H., Dorodnikov, M., Jones, D.L., Wu, J., Kuzyakov, Y., Nath, D.J., Ozah, B., Baruah, R., Barooah, R.C., Borah, D.K., 2011. Effect of integrated
2017. Rice rhizodeposition and its utilization by microbial groups depend on N nutrient management on soil enzymes, microbial biomass carbon and bacterial
fertilization. Biol. Fertil. Soils 53, 37–48. populations under rice (Oryza sativa) –wheat (Triticum aestivum) sequence. Ind. J.
Ge, Y., Zhang, J., Zhang, L., Yang, M., He, J., 2008. Long-term fertilization regimes affect Agric. Sci. 81, 1143–1148.
bacterial community structure and diversity of an agricultural soil in northern China. Nath, D.J., Ozah, B., Baruah, R., Barooah, R.C., Borah, D.K., Gupta, M., 2012. Soil
J. Soils Sediments 8, 43–50. enzymes and microbial biomass carbon under rice-toria sequence as influenced by
Gogoi, B., Barua, N.G., Baruah, T.C., 2010. Effect of integrated supply of nutrient on soil nutrient management. J. Ind. Soc. Soil Sci. 60, 20–24.
microbial biomass carbon in an Inceptisol of Assam. J. Ind. Soc. Soil Sci. 58, Navarro-Noya, Y.E., Gomez-Acata, S., Montoya-Ciriaco, N., Rojas-Valdez, A., Suarez-
241–244. Arriaga, M.C., Valenzuela-Encinas, C., Jimenez-Bueno, N., Verhulst, N., Govaerts, B.,
Gomez KA, Gomez AA. 1984. Statistical procedures for agricultural research. 2nd ed. Dendooven, L., 2013. Relative impacts of tillage, residue management and crop-
International Rice Research Institute. New York, Singapore: John Wiley and Sons. rotation on soil bacterial communities in a semi-arid agroecosystem. Soil Biol.
Institute Inc, S.A.S., 2013. SAS/STAT user’s Guide. SAS Institute Inc, Cary. Biochem. 65, 86–95.
Jackson, M.L., 1973. Soil Chemical Analysis. Prentice Hall of India Pvt. Ltd., New Delhi. Nayak, D.R., Babu, Y.J., Adhya, T.K., 2007. Longterm application of compost influences
Jackson, L.E., Bowles, T.M., Ferris, H., Margenot, A.J., Hollander, A., Garcia-Palacios, B., microbial biomass and enzyme activities in a tropical AericEndoaquept planted to
Daufresneg, T., Sánchez-Moreno, S., 2019. Plant and soil microfaunal biodiversity rice under flooded condition. Soil Bio. Biochem. 39, 1897–1906.
across the borders between arable and forest ecosystems in a Mediterranean Nayak, A.K., Gangwar, B., Shukla, A.K., Mazumdar, S.P., Kumar, A., Raja, R., Kumar, A.,
landscape. Appl. Soil Ecol. 136, 122–138. Kumar, V., Rai, P.K., Mohan, U., 2012. Long-term effect of different integrated
Jenkinson, D.S., Ladd, J.N., 1981. Microbial biomass in soil: measurement and turn over. nutrient management on soil organic carbon and its fractions and sustainability of
Soil Biochem. 5, 415–471. rice-wheat system in Indo Gangetic plains of India. Field Crop Res. 127, 129–139.
Jenkinson, D.S., Powlson, D.S., 1976. The effect of biocidal treatments on metabolism in Ndiaye, E.L., Sandeno, J.M., McGrath, D., Dick, R.P., 2000. Integrative biological
soil. V. A method for measuring soil biomass. Soil Biol. Biochem. 8, 209–213. indicators for detecting change in soil quality. Am. J. Altern. Agric. 15, 26–36.
Katkar, R.N., Sonune, B.A., Kadu, P.R., 2011. Long-term effect of fertilization on soil Othoniel, B., Rugani, B., Heijungs, R., Benetto, E., Withagen, C., 2016. Assessment of life
chemical and biological characteristics and productivity under sorghum (Sorghum cycle impacts on ecosystem services: promise, problems, and prospects. Environ. Sci.
bicolor)-wheat (Triticum aestivum) system in Vertisol. Ind. J. Agric. Sci. 81, Technol. 50 (3), 1077–1092.
734–739. Palm, C., Blanco-Canqui, H., DeClerck, F., Gatere, L., Grace, P., 2014. Conservation
Kaur, J., Choudhary, O.P., Singh, B., 2008. Microbial biomass carbon and soil properties agriculture and ecosystem services: an overview. Agr. Ecosyst. Environ. 187,
as influenced by long-term sodic water irrigation, gypsum and organic amendments. 87–105.
Aust. J. Soil Res. 46, 141–151. Patel, G., Dwivedi, B.S., Dwivedi, A.K., Thakur, R., Singh, M., 2018. Long-term effect of
Kundu, S., Bhattacharyya, R., Prakash, V., Ghosh, B., Gupta, H., 2007. Carbon nutrient management on soil biochemical properties in a Vertisol under
sequestration and relationship between carbon addition and storage under rainfed soybean–wheat cropping sequence. J. Ind. Soc. Soil Sci. 66, 215–221.
soybean-wheat rotation in a sandy loam soil of the Indian Himalayas. Soil Till. Res. Petrosillo, I., Valente, D., Pasimeni, M.R., Aretano, R., Semeraro, T., Zurlini, G., 2019.
92 (1-2), 87–95. Can a golf course support biodiversity and ecosystem services? The landscape
Kussainova, M., Durmus, M., Erkocak, A., Kizilkaya, R., 2013. Soil dehydrogenase context matter. Landscape Ecol. 34 (10), 2213–2228.
activity of natural macro aggregates in a topo-sequence of forest soil. Eurasian J. Soil Powlson, D.S., Prookes, P.C., Christensen, B.T., 1987. Measurement of soil microbial
Sci. 2, 69–75. biomass provides an early indication of changes in total soil organic matter due to
Ladd, J.N., Amato, M., Li-kai, Z., Schultz, J.E., 1994. Differential effects of rotation, plant straw incorporation. Soil Biol. Biochem. 19 (2), 159–164.
residue and nitrogen fertilizer on microbial biomass and organic matter in an Prakash, D., Benbi, D.K., Saroa, G.S., 2016. Effect of rate and source of phosphorus
Australian Alfisol. Soil Biol. Biochem. 26, 821–831. application on soil organic carbon pools under rice (Oryza sativa)-wheat (Triticum
Lee, S.B., Lee, C.H., Jung, K.Y., Park, K.D., Lee, D.P., Kim, J., 2009. Changes of soil aestivum) cropping system. Ind. J. Agric. Sci. 86, 1127–1132.
organic carbon and its fractions in relation to soil physical properties in a long-term Prakash, D., Benbi, D.K., Saroa, G.S., 2018. Land-use effects on phosphorus fractions in
fertilized paddy. Soil Till. Res. 104, 227–232. Indo-Gangetic alluvial soils. Agroforest. Syst. 92, 437–448.
Liang, Y.L., Chen, C., Xue, Q., Lin, X.J., Peng, Q., 2011. Long-term soil organic carbon Preethi, B., Poorniammal, R., Balachandar, D., Karthikeyan, S., Chendreyan, K.,
and crop yield dynamics in cropland in hilly and gully areas. Agron. J. 10, 40–47. Bhattacharyya, P., Adhya, T.K., 2013. Long-term organic nutrient managements
Liu, S., Costanza, R., Farber, S., Troy, A. 2010b. Valuing ecosystem services. Theory, foster the biological properties and carbon sequestering capability of a wetland rice
practice,and the need for a transdisciplinary synthesis. In: Limburg, K., Costanza, R. soil. Arch. Agron. Soil Sci. 59, 1607–1624.
(Eds.), Ecological Economics Reviews. Ann. Ny. Acad. Sci., pp. 54–78. Ramdas, M.G., Manjunath, B.L., Singh, N.P., Ramesh, R., Verma, R., Ashish, L.,
Liu, E., Yan, C., Mei, X., He, W., Bing, S.H., Ding, L., Liu, Q., Liu, S., Fan, T., 2010. Long- Marutrao, L.A., Ruenna, D., Natasha, B., Rahul, K., 2017. Effect of organic and
term effect of chemical fertilizer, straw and manure on soil chemical and biological inorganic sources of nutrients on soil microbial activity and soil organic carbon
properties in northwest China. Geoderma 158, 173–180. build-up under rice in west coast of India. 2017. Arch. Agron. Soil Sci. 63, 414–426.
Luo, P., Han, X., Wang, Y., Han, M., Shi, H., Liu, N., Bai, H., 2015. Influence of long-term Ramirez, K.S., Craine, J.M., Fierer, N., 2012. Consistent effects of nitrogen amendments
fertilization on soil microbial biomass, dehydrogenase activity, and bacterial and on soil microbial communities and processes across biomes. Glob. Chang. Biol. 18,
fungal community structure in a brown soil of northeast China. Ann. Microbiol. 65 1918–1927.
(1), 533–542. Rinot, O., Levy, G.J., Steinberger, Y., Svoray, T., Eshel, G., 2019. Soil health assessment:
Malik, A.A., Puissant, J., Buckeridge, K.M., Goodall, T., Jehmlich, N., Chowdhury, S., a critical review of current methodologies and a proposed new approach. Sci. Total
Gweon, H.S., Peyton, J.M., Mason, K.E., van Agtmaal, M., Blaud, A., Clark, I.M., Environ. 648, 1484–1491.
Whitaker, J., Pywell, R.F., Ostle, N., Gleixner, G., Griffiths, R.I., 2018. Land use Ros, M., Hernandez, M.T., Garcia, C., 2003. Soil microbial activity after restoration of a
driven change in soil pH affects microbial carbon cycling processes. Nat. Commun. 9, semi-arid soil by organic amendments. Soil Biol. Biochem. 35, 463–469.
3591. https://doi.org/10.1038/s41467-018-05980-1. Shahid, M., Nayak, A.K., Shukla, A.K., Tripathi, R., Kumar, A., Mohanty, S.,
Mandal, B., Majumder, B., Bandopadhyay, P.K., Hazra, G.C., Gangopadhyay, A., Bhattacharyya, P., Raja, R., Panda, B.B., 2013. Long-term effect of fertilizer and
Mishra, A.K., Chowdhuri, J., Saha, M.N., Kundu, S., 2007. The potential of cropping manure application on soil quality and yields in a sub-humid tropical rice-rice
systems and soil amendments for carbon sequestration in soil under long-term system. Soil Use Manag. 29, 322–332.
experiments in subtropical India. Glob. Chang. Biol. 13, 357–369. Sheoran, S., Dev, R., Antil, R.S., Mor, V.S., Grewal, K.S., 2020. Soil microbial properties
Mandal, M., Rout, K.K., Purohit, D., Majhi, P., Singh, M., 2018. Evaluation of rice-rice influenced with long term application of manures and fertilizers. Ind. J. Agric. Sci.
system on grain yield, chemical and biological properties of an acid Inceptisols. 90, 178–182.
J. Ind. Soc. Soil Sci. 66, 208–214. Shukla, G., Varma, A., 2011. Soil Enzymology. Springer, Berlin.
Manna, M.C., SubbaRao, A., Mandal, A., 2013. Maintenance of soil biological health Singh, M., Wanjari, R.H., Dwivedi, A., Dalal, R., 2012. Yield response to applied nutrients
under different crop production systems. Ind. J. Soil Cons. 4, 127–135. and estimates of N2 fixation in 33 year old soybean–wheat experiment on a Vertisol.
Marinelli, M.V., Valente, D., Scavuzzo, C.M., Petrosillo, I., 2021. Landscape service flow Experimental Agri. 48 (3), 311–325.
dynamics in the metropolitan area of Còrdoba (Argentina). J. Environ. Manage. 280, Smith, J.L., Paul, E.A., 1990. The Significance of Soil Microbial Biomass Estimation.
111714 https://doi.org/10.1016/j.jenvman.2020.111714. Marcel Dekker Inc, New York.
Marschner, P., Kandeler, E., Marschner, B., 2003. Structure and function of the soil Stockmann, U., Mark, A., John, A., Crawford, W., Field, D.J., Henakaarchchi, N.,
microbial community in a long-term fertilizer experiment. Soil Biol. Biochem. 35, Jenkins, M., Minasny, B., McBratney, A.B., Courcelles, V.R., Singh, K., Wheeler, I.,
453–461. Abbott, L., Angers, D.A., Baldock, J., Bird, M., Brookes, P.C., Chenu, C., Jastrow, J.
Martin, J.P., 1950. Use of acid rose Bengal and streptomycin in plate method for D., Lal, R., Lehmannj, J., O’Donnell, A.G., Parton, W.J., Whitehead, D.,
estimating soil fungi. Soil Sci. 69, 215–232. Zimmermann, M., 2013. The knowns, known unknowns and unknowns of
Murugan, R., Kumar, S., 2013. Influence of long-term fertilization and crop rotation on sequestration of soil organic carbon. Agri. Ecosys. Environ. 164, 80–99.
changes in fungal and bacterial residues in a tropical rice field soil. Biol. Fertil. Soils Subbiah, S.V., Ramamoorthy, K., Kumar, R.R.M., Singh, S.P., 2001. Studies on yield
49, 847–856. maximization through balanced nutrient ratios in irrigated low land rice. Rice
Nair, A., Ngouajio, M., 2012. Soil microbial biomass, functional microbial diversity, and Commun. Newsletter 46, 59–61.
nematode community structure as affected by cover crops and compost in an organic Sun, R., Zhang, X.-X., Guo, X., Wang, D., Chu, H., 2015. Bacterial diversity in soils
vegetable production system. Appl. Soil Ecol. 58, 45–55. subjected to long-term chemical fertilization can be more stably maintained with the
addition of livestock manure than wheat straw. Soil Biol. Biochem. 88, 9–18.

9
B. Gogoi et al. Ecological Indicators 132 (2021) 108262

Sushma, A.R., Basavaraja, P.K., Badrinath, M.S., Sridhara, S., 2007. Residual effect of Wang, J., Zhang, H., Li, X., Su, Z., Li, X., Xu, M., 2014. Effects of tillage and residue
integrated nutrient management with coir pith compost and other organics on incorporation on composition and abundance of microbial communities of a fluvo-
subsequent Ragi crop yield and chemical properties of vertisols. J. Ind. Soc. Soil Sci. aquic soil. Eur. J. Soil. Biol. 65, 70–78.
55, 500–504. Williams, A., Hedlund, K., 2013. Indicators of soil ecosystem services in conventional and
Tabatabai, M.A., Bremner, J.M., 1969. Use of pnitrophenyl phosphate for assay of soil organic arable fields along a gradient of landscape heterogeneity in southern
phosphatase activity. Soil Biol. Biochem. 1, 301–307. Sweden. Appl. Soil Ecol. 65, 1–7.
Tao, L., Sun, Z., He, C., Ge, X., Ouyang, Z., Wu, L., 2020. Changes in soil bacterial Wu, F., Dong, M., Liu, Y., Ma, X., An, L., Young, J.P.W., Feng, H., 2011. Effects of long-
community structure and microbial function caused by straw retention in the North term fertilization on AM fungal community structure and glomalin related soil
China Plain. Arch. Agron. Soil Sci. 66, 46–57. protein in the Loess Plateau of China. Plant Soil 342 (1-2), 233–247.
Thakur, R., Sawarkar, S.D., Vaishya, U.K., Singh, M., 2011. Impact of continuous use of Wu, H., Yang, T., Liu, X., Li, H., Gao, L., Yang, J., Li, X., Zhang, L., Jiang, S., 2020.
inorganic fertilizers and organic manure on soil properties and productivity under Towards an integrated nutrient management in crop species to improve nitrogen and
soybean-wheat intensive cropping of a Vertisol. J. Ind. Soc. Soil Sci. 59, 74–81. phosphorus use efficiencies of Chaohu Watershed. J. Clean. Prod. 272, 122765.
Tong, X., Xu, M., Wang, X., Bhattacharyya, R., Zhang, W., Cong, R., 2014. Long-term https://doi.org/10.1016/j.jclepro.2020.122765.
fertilization effects on organic carbon fractions in a red soil of China. Catena 113, Yadav, G.S., Datta, R., Pathan, S.I., Lal, R., Meena, R.S., Babu, S., Das, A., Bhowmik, S.N.,
251–259. Datta, M., Saha, P., Mishra, P.K., 2017. Effects of conservation tillage and nutrient
Trasar-Cepeda, C., Leiros, M.C., Seoane, S., Gil-Sotres, F., 2008. Hydrolytic enzyme management practices on soil fertility and productivity of rice (Oryza sativa L.)–rice
activities in agricultural and forest soils. Some implications for their use as indicators system in north- eastern region of India. Sustainability 9, 1816. https://doi.org/
of soil quality. Soil Biol. Biochem. 40, 2146–2155. 10.3390/su9101816.
Tripura, P., Polara, K.B., Shitab, M., 2018. Influence of long term fertilization on yield Yadav, G.S., Lal, R., Meena, R.S., Babu, S., Das, A., Bhowmik, S.N., Datta, M., Layak, J.,
and active pools of soil organic carbon in an Typic Haplustepts under groundnut- Saha, P., 2019. Conservation tillage and nutrient management effects on
wheat cropping sequence. Internat. J. Curr. Microbiol. App. Sci. 7, 781–794. productivity and soil carbon sequestration under double cropping of rice in north
Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. Microbial biomass measurements in eastern region of India. Ecol. Indic. 105, 303–315.
forest soils: the use of chloroform fumigation-incubation methods for strongly acidic Yan, X., Zhou, H., Zhu, Q.H., Wang, X.F., Zhang, Y.Z., Yu, X.C., Peng, X., 2013. Carbon
soil. Soil Biol. Biochem. 19, 697–702. sequestration efficiency in paddy soil and upland soil under long-term fertilization in
Verma, G., Mathur, A.K., 2009. Effect of integrated nutrient management on active pools southern China. Soil Till. Res. 130, 42–51.
of soil organic matter under maize-wheat system of a Typic Haplustept. J. Ind. Soc. Zhang, W.J., Wang, X.J., Xu, M.G., Huang, S.M., Liu, H., Peng, C., 2010. Soil organic
Soil Sci. 57, 317–322. carbon dynamics under long-term fertilizations in arable land of northern China.
Villarino, S.H., Studdert, G.A., Laterra, P., 2019. How does soil organic carbon mediate Biogeosci. 7, 409–425.
trade-offs between ecosystem services and agricultural production? Ecol. Indic. 103, Zhang, X., Xin, X., Zhu, A., Yang, W., Zhang, J., Ding, S., Mu, L., Shao, L., 2018. Linking
280–288. https://doi.org/10.1016/j.ecolind.2019.04.027. macro aggregation to soil microbial community and organic carbon accumulation
Visser, S., Parkinson, D., 1992. Soil biological criteria as indicators of soil quality: soil under different tillage and residue managements. Soil Till. Res. 178, 99–107.
microorganisms. Am. J. Altern. Agric. 7, 33–37. Zhao, S., Li, K., Zhou, W., Qiu, S., Huang, S., He, P., 2016. Changes in soil microbial
Walkley, A., Black, I.A., 1934. An examination of the degtjareff method for determining community, enzyme activities and organic matter fractions under long-term straw
soil organic matter and a proposed modification of the chromic acid titration return in north-central China. Agr. Ecosyst. Environ. 216, 82–88.
method. Soil Sci. 37 (1), 29–38.

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