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Soil carbon sequestration, plant nutrients andbiological activities affected by organic farming systemin tea (Camellia sinensis (L.) O. Kuntze) fieldsWen-Yan Hana, Jian-Ming Xub, Kang Weia, Ruan-Zhi Shia & Li-Feng Maa

a Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008,Chinab Institute of Soil and Water Resources and Environmental Science, Zhejiang University,Hangzhou 310058, ChinaPublished online: 12 Nov 2013.

To cite this article: Wen-Yan Han, Jian-Ming Xu, Kang Wei, Ruan-Zhi Shi & Li-Feng Ma (2013) Soil carbon sequestration, plantnutrients and biological activities affected by organic farming system in tea (Camellia sinensis (L.) O. Kuntze) fields, SoilScience and Plant Nutrition, 59:5, 727-739, DOI: 10.1080/00380768.2013.833857

To link to this article: http://dx.doi.org/10.1080/00380768.2013.833857

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ORIGINAL ARTICLE

Soil carbon sequestration, plant nutrients and biological activities affectedby organic farming system in tea (Camellia sinensis (L.) O. Kuntze) fields

Wen-Yan HAN1, Jian-Ming XU2, Kang WEI1, Ruan-Zhi SHI1 and Li-Feng MA1

1Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008, China and 2Institute of Soil and WaterResources and Environmental Science, Zhejiang University, Hangzhou 310058, China

Abstract

There is growing interest in investigations into soil carbon (C) sequestration, plant nutrients and biologicalactivities in organic farming since it is regarded as a farming system that could contribute to climatemitigation and sustainable agriculture. However, most comparative studies have focused on annual cropsor farming systems with crop rotations, and only a few on perennial crops without rotations, e.g. tea(Camellia sinensis (L.) O. Kuntze). In this study, we selected five pairs of tea fields under organic andconventional farming systems in eastern China to study the effect of organic farming on soil C sequestration,plant nutrients and biological activities in tea fields. Soil organic C, total nitrogen (N), phosphorus (P),potassium (K) and magnesium (Mg), available nutrients, microbial biomass, N mineralization and nitrifica-tion were compared. Soil pH, organic C and total N contents were higher in organic tea fields. Soil microbialbiomass C, N and P, and their ratios in organic C, total N and P, respectively, net N mineralization andnitrification rates were significantly higher in organic fields in most of the comparative pairs of fields.Concentrations of soil organic C and microbial biomass C were higher in the soils with longer periodsunder organic management. However, inorganic N, available P and K concentrations were generally lowerin the organic fields. No significant differences were found in available calcium (Ca), Mg, sodium (Na), iron(Fe), manganese (Mn), copper (Cu) and zinc (Zn) concentrations between the two farming systems. Thesefindings suggest that organic farming could promote soil C sequestration and microbial biomass size andactivities in tea fields, but more N-rich organic fertilizers, and natural P and K fertilizers, will be required forsustainable organic tea production in the long term.

Key words: carbon sequestration, conventional farming, microbial biomass, organic farming, tea.

INTRODUCTION

There is growing interest in soil carbon (C) sequestra-tion, plant nutrients and biological activities in organicfarming since it is regarded as a farming system thatcould contribute to climate mitigation and sustainableagriculture. Organic farming systems are not permittedto use synthetic chemicals, such as inorganic fertilizersand chemical pesticides; instead crop rotation withlegumes, green manures and compost are applied, and

biological pest control systems are adopted. Many stu-dies have shown that organic farming could improve soilhealth and productivity by increasing soil organic C,plant nutrients, biodiversity, microbial activities andeven higher food supply compared to conventional farm-ing systems (e.g. Mäder et al. 2002; Gosling andShepherd 2005; Badgley et al. 2007; Fließbach et al.2007; Leifeld and Fuhrer 2010; Gattinger et al. 2012).For example, Gattinger et al. (2012) found significantincreases in organically farmed soils of 0.18% soilorganic C concentrations, equivalent to 3.50 ± 1.08million gram (Mg) C ha–1 for organic C stocks, and0.45 ± 0.21 Mg C ha–1 y–1 for sequestration rates com-pared with conventional management. These resultswere obtained from a meta-analysis of the data from74 comparisons of organic vs. nonorganic farming

Correspondence: W. HAN, Tea Research Institute, ChineseAcademy of Agricultural Sciences, 9 South Meiling Road,Hangzhou 310008, China. Tel.: 0086-571-86650413. Fax:0086-571-86650056. Email: hanwy@mail.tricaas.comReceived 10 April 2013.Accepted for publication 8 August 2013.

Soil Science and Plant Nutrition (2013), 59, 727–739 http://dx.doi.org/10.1080/00380768.2013.833857

© 2013 Japanese Society of Soil Science and Plant Nutrition

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systems. Fließbach et al. (2007) found that soil microbialbiomass concentration and dehydrogenase activity weresignificantly higher, but the specific respiration ratelower in organic farming system than in conventionalfarming systems. Badgley et al. (2007) estimated, frommodel estimations, that organic farming could produceenough food on a global per capita basis to sustain thecurrent human population, and potentially an even lar-ger population, without increasing the agricultural landbase. But other studies have not found such differences,and obtained opposite results (Kirchmann et al. 2007;Connor 2008; Leifeld et al. 2009; Leifeld 2012). Becauseof these contradictory findings, the advantages and dis-advantages of organic farming systems vs. conventionalfarming systems remain controversial (Kirchmann et al.2007; Leifeld and Fuhrer 2010; Leifeld 2012). Thesestudies mainly focused on annual crops or on crop rota-tions, and there have been few studies on perennial cropswithout rotation in tropical and subtropical zones.Tea (Camellia sinensis (L.) O. Kuntze) is a major cash

crop and plays a very important role in both economicdevelopment and poverty reduction in tropical and sub-tropical regions. There were about 3.85 million ha ofland under tea cultivation in the world in 2011 (ITC2012). Tea is regarded as a healthy drink and publicconcerns over environmental health, food quality andsafety have led to an increasing interest in organic farm-ing practices. Organic tea production has increased veryrapidly in China in the last decade. About 45,000 ha oftea fields were under organic management, with produc-tion of 35,000 tons in China in 2011. This represents anincrease of 33 times in area and 43 times in productioncompared with that in 2000. Tea is a perennial crop andno crop rotation takes place in tea fields. Tea is also aleaf harvested crop and needs more nitrogen (N) thanother crops with seeds or fruits as final products. N is aleading limiting factor for plant growth and tea produc-tivity. However, long-term and over application of Nleads to soil acidification. Tea is an unusual crop becausethe soil becomes strongly acidified following planting oftea and soil pH generally continues to decrease with theincrease of stand age and tea productivity (Song and Liu1990; Han et al. 2007a). Soil microbial biomass andactivities are significantly affected by the productivityand the age of tea plants (Yao et al. 2000; Tokuda andHayatsu 2002; Xue et al. 2006; Han et al. 2007a).However, there are no reports of changes of soil organicmatter, plant nutrients, microbial biomass and activitiesin tea fields under organic management.In this study, we collected soil samples from five loca-

tions, each with organic and conventional farming sys-tems with different soil characteristics and durations oforganic farming practices, in the Zhejiang province, east-ern China. The main objectives were to evaluate the

changes in soil organic C, total N, phosphorus (P) andpotassium (K), available nutrients, microbial biomass,net N mineralization and nitrification under organic teafarming system. The aim was to provide new informa-tion on soil C sequestration and microbial biomass sizeand activities under organic farming system of the per-ennial crop, tea, without rotation.

MATERIALS AND METHODS

Site characteristicsSoil samples were collected from five pairs of farmslocated in the Zhejiang province, eastern China. Thisregion has a subtropical monsoon climate with a cleardivision of four seasons and abundant sunshine. Themean annual temperatures in the five locations arearound 16.5 to 17.7°C, ranging from 2°C in Januaryto 33°C in July, based on the last three decades from1981 to 2010. The mean annual precipitation rangesfrom 1326 to 1720 mm. About three quarters of thisrain falls during the tea growing season from March toSeptember. The soils are mainly red soils. Detailedinformation for the five tea farm locations is listed inTable 1.The selected farms have both organic and conventional

tea gardens. The organic tea gardens were converted fromconventional ones in different years. The farm of Shaoxin isa tea field undergoing conversion. It was also selected inorder to investigate the changes in soil quality from con-ventional to organic management. The fertilizers applied inthe organic and conventional systems are listed in Table 2.The organic fertilizers were applied twice a year in Mayand October in organic and conversional fields with 50%in each application. The mineral fertilizers were appliedwith four split dressings in February, May, July andOctober, and organic fertilizer was applied only inOctober in conventional fields. Soil tillage and weedingwas done together with the application of organic fertilizersin both organic and conversional fields. No pesticides orbio-pesticides such as the nuclear polyhedrosis virus,Bacillus thuringiensis and matrine, or coloured stickyplates or frequency trembler grid lamps were used eitherin organic and conversional fields to control pests, andchemical pesticides were applied in conventional fields asrequired. Other field managements, such as pruning andplucking, were the same as applied locally.

Soil sampling and treatmentFor each farm, 400 m2 representative tea fields underorganic, one under conversion (only in Shaoxin farm)and conventional management, respectively, wereselected for soil sampling in September 2007. In eachsampled field, three independent soil samples were

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taken using a soil auger between tea rows. Each inde-pendent sample consisted of eight random sub-samplesof 0–20 cm depth and mixed. Samples were transportedin plastic bags to the laboratory as soon as possible.Plant residues, roots, stones and obvious macrofaunawere removed by hand, then the soil was sieved at fieldmoisture < 2 mm and stored at 4°C before analysis. Sub-samples were air-dried and ground < 160 µm for chemi-cal analysis. Soil dry matter (105°C, 24 h) and waterholding capacity (WHC) were determined, then the bulk

soils were adjusted to ca. 40% WHC and pre-incubatedaerobically at 25°C in the dark with water and soda-limefor 7 d before analysis of microbial biomass, net Nmineralization and nitrification.

Soil analysisSoil pHwas determined using a combined glass electrode in1:1 [weight:volume (w/v)] ratio of soil with distilled water.Soil organic C (Corg) and total N (Ntot) were determined bya Vario Max CN Analyzer (Elementar Analysensysteme

Table 2 Fertilization employed and mean tea (Camellia sinensis (L.) O. Kuntze) productivity in organic and conventional tea fieldsat five farms studied

Farm Management Fertilizers and their quantities applied annually

Average yieldafter start of

organicmanagement(kg ha–1)

Wuyi Organic Commercial organic fertilizer 9000 kg ha–1 for 11 years 4333Conventional Commercial organic fertilizer 4500 kg ha–1, mineral nitrogen (N),

phosphorus pentoxide (P2O5) and potassium oxide (K2O) 600,200 and 200 kg ha–1, respectively

4667

Yiwu Organic Rape seed cake 4500 or compost 6000 kg ha–1 for 9 years 2396Conventional Rape seed cake 2250 kg ha–1, mineral N, P2O5

and K2O 450, 225 and 225 kg ha–1, respectively2605

Shaoxin Organic Compost 9000 kg ha–1 for 8 years 1739Conversional Compost 12000 kg ha–1 for 2 years 1643Conventional Compost 6000 kg ha–1, mineral N, P2O5 and K2O 600, 300 and

300 kg ha–1, respectively. Additional super phosphate appliedsometimes

1819

Lanxi Organic Rape seed cake 4500 or compost 6000 kg ha–1 for 6 years 2775Conventional Compost 3000 kg ha–1, mineral N, P2O5 and K2O 450, 225

and 225 kg ha–1, respectively3150

Jiangshan Organic Compost 6000 kg ha–1 for 3 years 2510Conventional Mineral N, P2O5 and K2O 450, 225 and 225 kg ha–1, respectively 2987

Table 1 Selected information for the five experimental tea (Camellia sinensis (L.) O. Kuntze) fields located in Zhejiang province,China

Farm siteSite

location

Mean annualtemperature

(°C)

Mean annualprecipitation

(mm)Standing age oftea trees (years)

Year startingorganic

managementSoil parentmaterial

Claycontent(%)

US soilclassification

Wuyi 119°59′ E28°61′N

16.9 1446 60 1996 Basalt 47.8 Ultisols

Yiwu 120°09′ E29°47′N

17.1 1326 50 1998 Sand stone 30.8 Ultisols

Shaoxin 120°71′ E29°95′N

16.5 1440 40 1999 Tuff 33.5 Ultisols

Lanxi 119°50′ E29°14′N

17.7 1440 30 2001 Quaternaryclay

52.3 Oxisols

Jiangshan 118°50′ E28°62′N

17.1 1720 20 2004 Basalt 43.6 Oxisols

Soil quality under organic tea management 729

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GmbH,Germany). Soil total P (Ptot) andKwere determinedfollowing digestion with a mixed solution of hydrofluoricacid, perchloric acid and concentrated nitric acid (HF-HClO4-HNO3) by using inductively coupled plasmaatomic emission spectroscopy (ICP-AES) (JAC IRIS/AP,Thermo Jarrell Ash Corporation, Franklin, USA). Soilavailable P were extracted by Bray-1 solution (0.03 Mammonium fluoride (NH4F) + 0.025 M hydrochloric acid(HCl)) and available potassium (K), calcium (Ca), magne-sium (Mg) and sodium (Na) by 1 M ammonium acetate(NH4OAC), at a 1:10 soil-solution ratio for 0.5 h. Soilavailable iron (Fe), manganese (Mn), copper (Cu) andzinc (Zn)were extracted by0.1MHCl at a 1:5 soil-solutionratio for 1 h. These elements were analyzed by ICP-AES.Soil microbial biomass C, N (expressed as ninhydrin-N)

and P were determined by the fumigation-extractionmethod (Brookes et al. 1985; Vance et al. 1987; Wuet al. 1990). Three replicates of both fumigated and non-fumigated soils were extracted with 0.5 M potassiumsulphate (K2SO4) for 30 min (1:4 soil:extractant ratio).Organic C was measured by automated liquid organic Canalysis. Microbial biomass C (Cmic) was calculated from:

Cmic ¼ Ec=kc (1)

where Ec = [(organic C extracted from fumigated soil)minus (organic C extracted from non-fumigated soil)]and kc = 0.45. Biomass ninhydrin-N (Nninmic) concen-trations were measured colorimetrically (Joergensen andBrookes 1990; Amato and Ladd 1994). Microbial bio-mass phosphorus (Pmic) was determined by the methodof Wu et al. (2000). Soil samples were extracted by Bray-1 solution with a soil to solution ratio of 1:4 (w/v) for 30min. The P concentrations were determined colorimetri-cally at 710 nm. Pmic was calculated from

Pmic ¼ Ep= kp� Rð Þ (2)

where Ep = (inorganic P (Pi) extracted from chloroform(CHCl3) fumigated soil) minus (Pi extracted from nonfumigated soil); kp (the fraction of soil microbial Pextracted from soil following fumigation) = 0.4 and R =%of inorganic P recovered from a spike of added inorganicP extracted from a non fumigated soil (Brookes et al.1982). R ranged from 5 to 99% in the tested soils.N mineralization was determined by aerobic incubation

of replicate portions of bulk soils at 25°C in drums contain-ing distilled water and soda-lime. After 0, 7, 14, 21 and 35d, sub-samples were extracted with 0.5 M K2SO4 for 30min (soil:extractant ratio of 1:4) and analysed for mineralN (ammonium (NH4

+), nitrate (NO3–)) by Flow Injection

Analysis (Skalar SAN++ system, Netherlands). Net rates ofNmineralization and nitrification were calculated from thechanges in total mineral N and NO3

–-N pool sizes, respec-tively, during the incubations.All results are expressed on an oven-dry soil basis (105°

C, 24 h) and are the means of three replicate analyses.

Statistical analysesThe data were subject to one-way and two-way analysis ofvariance (ANOVA) by SPSS 13 for Windows. One-wayANOVA was used to compute means and least significantdifferences (LSD) with different management systems as afactor in different farms, with the significance level set at p< 0.05. Two-way ANOVA was performed to test farm siteandmanagement system effects. All the figures aremade bySigmaPlot 11.0 and exported in TIFF format.

RESULTS

Soil pH, organic C, total N, P, K and MgThe soil pH, organic C, total N, P, K and Mg contents inthe five tea farms with different management systems arelisted in Table 3. The soil pH and the contents of organicC and total N were consistently higher in organic than inconventional fields, although most differences were notstatistically significant due to high variation of soil sam-ples. In the Shaoxin farm, the soil pH was 4.21 followingorganic management for 8 years, significantly higherthan the pH of 3.86 under conventional management,and the conversion soil was midway at pH 4.05. Thedifferences in organic C and total N between the organicand the conventional fields were statistically significantat Wuyi farm, the oldest field under organic manage-ment. A significant relationship was found between thepercentage increases of soil organic C and age of teafields under organic management (Fig. 1). On average,the organic C and total N in organic fields wereincreased by 7.2 and 7.7%, respectively, comparedwith the conventional fields. However, the total P wasquite different and higher in most of the conventionalfields. In the Shaoxin and Wuyi sites, a significant differ-ence was found due to superphosphate applied in theconventional fields. The soil total K and Mg concentra-tions in the different managements were not significantlydifferent though a little lower in organic fields in mostpairs of soils.

Soil available nutrientsThe soil available P, K, Ca, Mg, Na, Fe, Mn, Cu and Znconcentrations in the tea fields with different management

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systems in five farms are listed in Table 4. Except foravailable K in Jiangshan farm, the available P and K con-centrations were lower in the organic fields due to theapplication of chemical P and K fertilizers in the conven-tional fields. There were significant differences betweenconventional and organic systems in available P in Yiwu,Shaoxin, Lanxi and Jiangshan farms, and available K inWuyi. The same trend did not occur in available Ca, Mgand Na concentrations. Significantly higher available CaandMgwere found only in the conventional field ofWuyi,the longest under organicmanagement. The concentrationsof available Fe,Mn, Cu andZnwere generally higher in theorganic fields than in the conventional fields. The Fe andZn concentrations in the organic fields in Shaoxin farmwere significantly higher as was the Cu concentration inWuyi farm than the conventional fields. An opposite resultalso occurred in soils of Jiangshan farm, while the concen-trations of Fe and Cu were significantly lower in theorganic fields. However, two-way ANOVA test resultsshowed no significant differences between organic andconventional farming systems for all these available metalelements (Table 4).

Microbial biomass C, N, P and their contribu-tion to organic C, total N and PThe different management systems had great impacts onthe size of the microbial communities in soils under teacultivation (Fig. 2). Microbial biomass C, N and P insoils of organic fields were significantly higher than thosein conventional fields in Wuyi and Shaoxin farms. Therewere also significant differences in biomass N and P inYiwu farm, and biomass P in Lanxi farm. In othercomparative pairs, the biomasses were all higher inorganic fields although the differences were not statisti-cally significant. This was so even at Jiangshan farm,where the organic management system was onlyemployed for 3 years. There was a significant positivelinear correlation between percentage increase in soilmicrobial biomass C and age of tea fields under organicmanagement (Fig. 3).The ratios of Cmic:Corg, Nninmic:Ntot and Pmic:Ptot

under the different management systems are shown inFig. 4. These ratios were higher in organic fields than inconventional ones. Significant or noticeable differenceswere found in Wuyi, Yiwu and Shaoxin farms, where theorganic management system was employed for at least 8years. These ratios in the conversion field in Shaoxinfarm were mid-way between conventional and organicfields, indicating that the organic farming system had apositive impact on the size of the soil microbialcommunities.The results of two-way ANOVA with farm site and

management system as factors also showed significantTab

le3

SoilpH

,orga

niccarbon

(C),totalnitrog

en(N

),ph

osph

orus

(P),po

tassium

(K)an

dmag

nesium

(Mg)

contents

inthefields

underdifferentman

agem

entsystem

sin

five

farm

s

Farm

(F)

Man

agem

ent(M

)pH

(H2O)

Organ

icC

(gkg

–1)

Total

N(g

kg–1)

Total

P(g

kg–1)

Total

K(g

kg–1)

Total

Mg(g

kg–1)

Wuy

iOrgan

ic3.86

±0.11

19.1

±0.3a

1.89

±0.04

a0.56

±0.03

a7.66

±0.20

1.91

±0.10

Con

ventiona

l3.53

±0.07

17.5

±0.2b

1.70

±0.02

b0.73

±0.03

b7.93

±0.16

2.05

±0.07

Yiw

uOrgan

ic4.40

±0.30

14.2

±0.8

1.23

±0.09

0.57

±0.08

8.00

±0.05

2.17

±0.10

Con

ventiona

l3.72

±0.12

13.3

±1.5

1.00

±0.06

0.50

±0.11

8.12

±0.19

2.19

±0.05

Shao

xin

Organ

ic4.21

±0.08

a20

.7±1.7

1.63

±0.09

0.45

±0.07

a10

.51±0.30

2.53

±0.05

Con

versiona

l4.05

±0.08

a18

.2±1.5

1.47

±0.01

0.64

±0.08

a10

.62±0.23

2.48

±0.03

Con

ventiona

l3.86

±0.01

b18

.7±0.4

1.53

±0.15

1.45

±0.12

b11

.23±0.47

2.63

±0.14

Lan

xiOrgan

ic3.95

±0.21

14.7

±0.6

1.15

±0.15

1.07

±0.33

7.71

±0.12

1.88

±0.03

Con

ventiona

l3.73

±0.24

14.3

±3.6

1.20

±0.10

1.57

±0.02

7.87

±0.02

1.88

±0.03

Jian

gsha

nOrgan

ic4.07

±0.05

9.6±0.3

0.70

±0.00

0.36

±0.01

7.96

±0.25

4.22

±0.08

Con

ventiona

l3.81

±0.08

9.3±0.3

0.70

±0.00

0.35

±0.00

7.60

±0.51

4.07

±0.08

ANOVA

test

(Fva

lue)

Factor

F2.30

20.84*

**47

.20*

**23

.58*

**63

.23*

**22

1.33

***

M12

.23*

*1.79

1.89

17.21*

**0.00

0.09

F×M

0.88

0.16

1.16

11.02*

**0.56

1.23

Means

arepresented±stan

dard

error(SE).The

follo

wingdifferentletterswithinacolumnin

thesamefarm

deno

tesign

ificant

difference

(p<0.05

)betw

eenfieldman

agem

ents.T

heda

taof

conv

ersion

alman

agem

entin

Shao

xinfarm

wereexclud

eddu

ring

thetw

o-way

analysisof

varian

ce(A

NOVA)test.*,

**,**

*afterFvaluemeanp<0.05

,0.01

and0.00

1,respectively.

Soil quality under organic tea management 731

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differences among sites and between farming systems. Thisindicates that organic farming could significantly increasethe microbial biomass in tea fields (Figs. 2 and 4).

Net N mineralization and nitrificationThe initial soil NH4

+, NO3– concentrations, net N miner-

alization and nitrification rates in the soils under differ-ent management systems are listed in Table 5. The initialNO3

–-N concentrations were significantly lower in thesoils of the organic tea fields compared to the conven-tional fields in all five farms. The NH4

+-N concentrationswere also significantly lower in the Yiwu, Lanxi andJiangshan farms under organic management due to theapplication of urea in the conventional fields. However,the soil net N mineralization and nitrification rates underorganic management were higher in most of the com-parative pairs. Opposite results were also found in Yiwuand Jiangshan farms with conventional fields havingsignificantly higher nitrification rates. This was probablydue to the significantly higher concentrations of NH4+-N, the substrate of nitrification in these two fields.

DISCUSSION

Soil pH and C sequestrationSoil pH is a primary regulator of soil nutrient cycling.There are few reactions involving soil or its biology thatare not affected by soil pH, and this sensitivity must be

recognized in any soil-management system. Higher soilpH is typically observed in organic compared to conven-tional management (Reganold et al. 1993; Clark et al.1998; Fließbach et al. 2007). The present study is con-sistent with these findings. Soil pH in organic manage-ment was higher in all five comparative pairs, and therewere significant differences between management typesin a two-way ANOVA analysis (Table 3). It is under-standable that organic fertilizers can increase soil buffer-ing capacity and prevent pH swings in soils, but thechemical fertilizers, especially N fertilizers, cause soilacidification. The raising of soil pH is beneficial to bal-ance nutrient availability and improve soil biodiversity,since pH in tea soils is too low and the pH of about 50%of tea soils is less than 4.5 in the typical tea-producingregions in China (Han et al. 2002).Organic farming is believed to improve soil fertility by

enhancing soil organic matter content. The present studydemonstrated that soil organicCwas significantly or obser-vably higher in the soils under organic management. Soilorganic C was increased by 7.2% compared to the conven-tional fields, expressed as a mean over the five comparablepairs. The mean organic matter content was 6.4% higherin organic managed fields than the conventional ones,calculated from a meta-analysis (Mondelaers et al. 2009).The current study also showed that the longer the field washeld under organic management, the higher was the soilorganic C. A significant relationship was found betweenthe percentage increase in soil organic C and age of teafields under organic management (Fig. 3). These results

Figure 1 Relationship between percentage increase in soil organic carbon (C) and age of tea (Camellia sinensis (L.) O. Kuntze) fieldsunder organic management. The line is predicted relationship and points are % increases in soil organic C in the fields under organicmanagement compared to the conventional management from the tested farms.

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indicate that organic tea cultivation could improve soil Csequestration without the use of rotations. This could beattributed to the following mechanisms:T

able

4Con

centration

sof

availablenu

trientsin

thefields

ofdifferentman

agem

entsystem

sin

five

farm

s(m

gkg

–1)

Farm

(F)

Man

agem

ent

(M)

Phosph

orus

(P)

Potassium

(K)

Calcium

(Ca)

Mag

nesium

(Mg)

Sodium

(Na)

Iron

(Fe)

Man

ganese

(Mn)

Cop

per

(Cu)

Zinc

(Zn)

Wuy

iOrgan

ic73

.1±15

.164

.7±4.5a

191.5±2.5a

20.0

±1.9a

13.6

±1.0

39.8

±4.4

33.0

±3.7

2.65

±0.09

a11

.48±1.42

Con

ventiona

l10

4.1±8.1

154.6±3.3b

230.6±5.8b

29.5

±1.5b

12.6

±0.3

32.6

±1.5

35.6

±5.4

2.09

±0.11

b8.12

±0.10

Yiw

uOrgan

ic21

.3±4.9a

66.2

±10

.022

1.1±12

.338

.9±5.0

27.8

±4.3

37.5

±14

.042

.6±15

.02.62

±0.80

18.73±5.34

Con

ventiona

l11

3.5±11

.5b

166.6±44

.632

5.1±78

.277

.7±35

.132

.7±1.3

44.4

±21

.417

.5±10

.11.71

±0.04

16.45±2.01

Shao

xin

Organ

ic14

.4±2.2a

116.0±6.1

274.5±30

.432

.9±2.1

27.9

±2.5

75.9

±4.7a

89.1

±5.5

3.96

±0.20

11.22±0.49

aCon

versiona

l61

.4±11

.0b

92.1

±24

.418

4.8±48

.335

.2±8.

428

.8±1.2

54.4

±21

.2ab

65.2

±15

.73.42

±0.88

11.70±0.47

aCon

ventiona

l11

3.2±22

.1c

146.5±19

.524

4.4±26

.650

.1±9.4

32.0

±1.4

25.2

±2.4b

62.6

±4.6

2.44

±0.07

8.27

±0.35

bLan

xiOrgan

ic19

.4±7.0a

121.0±13

.026

8.1±78

.157

.4±15

.533

.8±2.0

36.4

±5.3

33.7

±19

.01.85

±0.06

16.61±0.92

Con

ventiona

l10

4.6±16

.4b

139.0±3.4

352.5±65

.837

.7±6.0

31.2

±1.1

37.0

±5.2

122.5±57

.74.00

±2.10

15.05±3.95

Jian

gsha

nOrgan

ic17

.9±1.5a

282.1±32

.027

4.0±49

.674

.0±28

.742

.6±7.0

21.6

±0.7a

57.2

±12

.11.62

±0.01

a14

.76±2.48

Con

ventiona

l26

.1±0.8b

240.2±9.3

214.7±11

.744

.4±2.3

34.6

±0.3

32.1

±1.4b

20.8

±0.5

2.04

±0.01

b9.09

±0.25

ANOVA

test

(Fva

lue)

Factor

F6.83

**22

.35*

**1.42

1.71

41.85*

**1.37

4.52

*1.90

4.31

*M

40.71*

**2.10

1.03

0.10

0.14

3.49

0.00

2.09

1.47

F×M

12.10*

**3.35

*1.34

1.45

2.94

2.74

4.36

*2.72

0.79

Means

arepresented±stan

dard

error(SE).The

follo

wingdifferentletterswithinacolumnin

thesamefarm

deno

tesign

ificant

difference

(p<0.05

)betw

eenfieldman

agem

ents.T

heda

taof

conv

ersion

alman

agem

entin

Shao

xinfarm

wereexclud

eddu

ring

thetw

o-way

analysisof

varian

ce(A

NOVA)test.*,

**,**

*afterFvaluemeanp<0.05

,0.01

and0.00

1,respectively.

Figure 2 Soil microbial biomass carbon (C), ninhydrin-nitrogen(N) and phosphorus (P) in tea (Camellia sinensis (L.) O. Kuntze)fields under different management systems. Vertical bars are stan-dard errors. Different letters denote significant differences (p <0.05) between management in the same farm. The analysis ofvariance (ANOVA) results are inset. S, experimental sites; M,management systems. The data of conversional management inShaoxin farm were excluded during the two-way ANOVA test. *,**, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

Soil quality under organic tea management 733

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1. Higher organic C input rate. Ameta-analysis showed thatthe highest C sequestration was achieved by those prac-tices supplying the largest C inputs (Aguilera et al.2013). Without manure application, organic C coulddecline by 14–22% in a 21-year long-term experiment(Fließbach et al. 2007). In this study, the organic teafields received almost twice as much organic fertilizeras did the conventional fields.

2. Conservation tillage practices. No-tillage or reducedtillage could significantly promote C sequestration.No tillage showed an average increase of 11.4% insoil organic C and 0.44 Mg C ha–1 yr–1 in C seques-tration rate (Aguilera et al. 2013).

3. Lower microbial biomass C specific respiration rate(SRR), defined as:

SRR ¼ ½ CO2 � C evolved in time tð Þ=microbial biomass Cð Þ (3)

Compared to conventional farming systems, organicfarming could cause a decrease of 21% in the specificrespiration rate (Fließbach et al. 2007). Tea soil has alower specific respiration rate than other soils grow-ing vegetables, citrus, paddy and forest, which is alsobeneficial to C accumulation and soil qualityimprovement (Yao et al. 2000; Han et al. 2007a).

Soil total and available nutrientsPlant growth and ecosystem productivity are signifi-cantly affected by the availability of plant nutrients,

with N, P and K being the main growth-limiting nutri-ents for plant production. N is stored in soil primarily inorganic matter, from which it is mineralized to ammo-nium-N by the action of soil micro-organisms. Organicfarms rely heavily on soil biological activity and croprotation with legume crops to provide N to plants(Mäder et al. 2002; Tu et al. 2006; Fließbach et al.2007; Moeskops et al. 2010). Tea is a leaf harvestedmono perennial crop and large amounts of N fertilizerare applied in conventional tea fields (Tokuda andHayatsu 2000; Han and Li 2002). However, chemicalfertilizer is not permitted in organic tea fields. Thereforesufficient plant nutrients, particular N availability for teagrowth and quality, are often a concern for organic teaproducers. The present study showed that soil total Ngradually increased due to the higher application rate oforganic fertilizers. However, N availability, i.e. themineral N concentration, was significantly lower in thesoils of organic tea fields compared to that in the con-ventional fields, thought there is generally higher miner-alization and nitrification rates in soils from organicfields. It was lowest in the Wuyi organic tea field, thefarm under the longest organic management. The meanyield of organic tea fields was 10% lower than that ofthe conventional fields in this study (Table 2), indicatingthat the mineral N absorbed by tea plants was lower inthe organic tea fields. These results show that the mineralN supply is insufficient in organic tea fields, though thesoils receive a greater amount of organic fertilizers andhave higher mineralization rates compared to the

Figure 3 Relationship between percentage increase in soil microbial biomass carbon (C) and age of tea (Camellia sinensis (L.) O.Kuntze) fields under organic management. The line is predicted relationship and points are % increases in soil microbial biomass C inthe fields under organic management compared to the conventional ones from the tested farms.

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conventional fields. In addition, the total P and K andavailable P and K concentrations in organic fields weregenerally lower due to non-application of mineral

fertilizers. Other studies also showed that organic man-agement could utilize reserves of P and K, accumulatedduring conventional management (Oehl et al. 2002;Gosling and Shepherd 2005).The available Ca, Mg, Na and Mn concentrations

were the same in the two farming systems in our study.However, Clark et al. (1998) and Bulluck et al. (2002)reported that these elements were higher in organic farm-ing systems. The difference is probably because the per-iod under organic management in our study wasinsufficient since some available nutrients decreasedafter converting to organic management, but increasedunder longer periods of organic management (Coll et al.2011). These results indicate that the low yield oforganic tea is probably due to the limitation of availablenutrients, especially N, P and K. Therefore, it is impor-tant in organic tea fields that a relatively large amount ofN-rich organic fertilizers, and sufficient natural P and Kfertilizers, should be applied in order to insure a suffi-ciently high yield in the long term.

Soil microbial biomass size and microbialactivitiesThe soil microbial biomass is both a labile nutrient pooland an agent of transformation and cycling of organicmatter and plant nutrients in soils. It is one of the mostimportant soil organic fractions although comprisingonly a small proportion (typically 1–5%) of soil organicmatter (Sparling 1997). It responds more rapidly tochanges in soil management than soil organic matterand, consequently, may provide an early and sensitiveindicator of soil quality change (Sparling 1992; Zagal2009). The proportion of microbial biomass C relative tosoil organic C has been used as an indicator of C avail-ability (Insam and Domsch 1988; Yan et al. 2003) andcan also provide an effective early indicator of theimprovement or deterioration of soil quality. The presentstudy showed that organic management can significantlyincrease soil microbial biomass C, ninhydrin-N and bio-mass P contents compared to conventional farming sys-tems. More importantly, the ratios of Cmic:Corg, Nninmic:Ntot and Pmic:Ptot were significantly or noticeable higherin the organic fields than in the conventional ones. In theconversion field of Shaoxin, these ratios were mid-waybetween those in conventional and organic fields, indi-cating that changing from conventional to organic farm-ing system increased the size of the microbial biomass.There was a significant positive relationship between theincrease in soil microbial biomass C and age of tea fieldsunder organic management (Fig. 4), These results areconsistent with previous findings (Fließbach and Mäder2000; Araujo et al. 2008; Coll et al. 2011), indicatingthat perennial tea crop under organic farming system can

Figure 4 Ratios of soil microbial biomass carbon (C), ninhydrin-nitrogen (N) and biomass phosphorus (P) to organic C, total N andP, respectively, under the different management systems. Verticalbars are standard errors. Different letters denote significant differ-ences (p < 0.05) betweenmanagement in the same farm. The analysisof variance (ANOVA) results are inset. S, experimental sites; M,management systems. The data of conversional management inShaoxin farm were excluded during the two-way ANOVA test. *,**, *** after F value mean p < 0.05, 0.01 and 0.001, respectively.

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improve soil quality. The higher microbial size and ratiosof Cmic:Corg, Nninmic:Ntot and Pmic:Ptot in the organicfields were attributed to higher organic matter contentsand increasing soil pH (Yao et al. 2000; Han et al.2007a). They were also attributed to no use of herbicidesand pesticides (Muñoz-Leoz et al. 2011). Blagodatskayaand Anderson (1999) found that at soil pH 3, biomass Cwas only 0.5% of organic C, but it was 2.4% at pH 7.We found that the soil pH was significantly related toCmic (r = 0.645, n = 33, p < 0.001) and the ratio of Cmic:Corg (r = 0.655, n = 33, p < 0.001), and total organic Cwas significantly related to Cmic (r = 0.510, n = 33,p < 0.01) and Pmic (r = 0.618, n = 33, p < 0.001). Thismay be related to the effects of soil pH on substrateavailability for microorganisms. Several mechanismsmay account for this:

1. Metabolic functions of the soil microorganisms maybe impaired by lower soil pH, directly via protontoxicity or by larger concentrations of availabletoxic metals. A greater proportion of heavy metalsare complexed on soluble organic matter at highersoil pHs. These heavy metals tend to become bioa-vailable and have increased toxicity as soil pHdeclines (Sanders 1983; Han et al. 2006, 2007b).

2. Low pH may cause changes in the chemical config-uration and reactions of humic substances (Schnitzer1980). Humic and fulvic acids aggregate at low pHbecause of hydrogen bonding, van der Waal’s inter-actions, interactions between π electrons of adjacentmolecules and homolytic reactions between free radi-cals. At higher pH, these forces are weaker andincreased ionization of carboxylic acids and phenolic

hydroxyl groups cause particles to separate and repeleach other, resulting in smaller and more orientedmolecular arrangements (Schnitzer 1980).

3. Application of large amount of chemical fertilizers,especially N fertilizers, lowers soil pH, whichdecreases biomass concentrations (Nioh et al. 1993;Ge et al. 2010). Thus, the tea soil received three timesthe rate of N (1200 kg N ha–1 as ammonium sulphate)yet contained only 17% of biomass C compared tothe soil receiving standard N application (Nioh et al.1993).

4. Tea roots exude large quantities of organic acids, suchas oxalic acid, citric acid and malate. These contributeto localized acidification (Wang 1994), which sup-presses the microbial biomass (Pandey and Palni1996).

The microbial mineralization of soil organic matter,manure or litter to ammonium and nitrate are the prin-cipal sources of plant available N in organic farmingsystems since no inorganic N fertilizer is applied. It wasestimated that 50% of crop N uptake on average inconventional systems is derived from fertilizers in theyear of application with the remainder from mineraliza-tion of soil organic matter (Jarvis et al. 1996). In organicfarming systems, with an absence of soluble fertilizers,the importance of mineralization in the supply of nutri-ents to plants is clearly increased. Therefore, the rates ofmineralization and nitrification play a key role in the Ncycle by making N available for plants and microbes inthe soils (Fließbach and Mäder 2000). Not only theavailable N, but the available P and K in the soil solutionpool are partly derived from the mineralization of soil

Table 5 Soil net nitrogen (N) mineralization and nitrification rates under different management systems in five farms

Farm (F)Management

(M)

Initial ammonium(NH4

+)-N(mg kg–1)

Initial nitrate (NO3–)-N

(mg kg–1)Mineralization rate

(mg kg–1 d–1)Nitrification rate(mg kg–1 d–1)

Wuyi Organic 2.0 ± 0.2 13.8 ± 0.5 a 0.68 ± 0.07 1.03 ± 0.10 aConventional 1.8 ± 0.4 52.6 ± 5.4 b 0.44 ± 0.09 0.59 ± 0.02 b

Yiwu Organic 3.9 ± 0.2 a 35.8 ± 2.6 a 0.62 ± 0.06 a 0.54 ± 0.05 aConventional 57.8 ± 5.3 b 130.0 ± 4.9 b 1.19 ± 0.18 b 1.93 ± 0.17 b

Shaoxin Organic 2.3 ± 0.1 20.4 ± 2.8 a 1.35 ± 0.21 a 1.29 ± 0.20 aConversional 2.4 ± 0.1 24.4 ± 2.8 a 0.79 ± 0.08 b 0.77 ± 0.08 bConventional 2.5 ± 0.0 60.2 ± 10.0 b 0.69 ± 0.06 b 0.67 ± 0.06 b

Lanxi Organic 17.8 ± 2.5 a 31.8 ± 3.5 a 1.44 ± 0.06 a 2.00 ± 0.07 aConventional 38.5 ± 1.4 b 245.0 ± 29.2 b 1.15 ± 0.08 b 1.37 ± 0.08 b

Jiangshan Organic 14.8 ± 1.6 a 35.9 ± 0.5 a 3.54 ± 0.20 a 2.67 ± 0.03 aConventional 50.8 ± 1.8 b 144.5 ± 0.4 b 1.90 ± 0.09 b 3.20 ± 0.06 b

ANOVA test (F value)

Factor F 115.9*** 35.1*** 120.9*** 146.3***M 289.6*** 237.6*** 44.3*** 0.6F × M 64.4*** 24.6*** 27.7*** 40.2***

Means are presented ± standard error (SE). The following different letters within a column in the same farm denote significant difference (p < 0.05) between fieldmanagements. The data of conversional management in Shaoxin farm were excluded during the two-way analysis of variance (ANOVA) test. *, **, *** after Fvalue mean p < 0.05, 0.01 and 0.001, respectively.

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organic matter and crop residues (Stockdale et al. 2002).The present study shows that soil net N mineralizationand nitrification rates under organic management werehigher than these in some of the fields under conven-tional management. However, the opposite results werealso found in Yiwu and Jiangshan farms with conven-tional fields having significantly higher nitrification rates(Table 5). This is probably because the chemically Nfertilized soils have a higher nitrification substrate, nitri-fying activity and an accelerated growth of the nitrifyingpopulation (Chu et al. 2008; Gong et al. 2011; Han et al.2012). In this study, we found these two farms hadhigher initial NH4

+-N compared to other sites, and theinitial NH4

+-N concentration was significantly correlatedwith the nitrification rate (r = 0.683, n = 11, p < 0.05).

CONCLUSIONS

Soil pH, organic C and total N contents were higher inthe organic fields mainly due to higher inputs of organicfertilizer and no chemical fertilizers used. The microbialbiomass C, ninhydrin-N and biomass P, and the ratios ofCmic:Corg, Nninmic:Ntot, Pmic:Ptot, the net N mineraliza-tion and nitrification rates were significantly higher inthe organic fields in most of the comparative pairs. Thelonger the field was under organic management, themore organic C and microbial biomass C were present.However, inorganic N, available P and K concentrationswere generally lower in organic fields. No significantdifferences were found in available Ca, Mg, Na, Fe,Mn, Cu and Zn concentrations between the two farmingsystems. These findings suggest that organic farmingcould promote soil C sequestration and microbial bio-mass size and activities in tea fields without crop rota-tion, but more N-rich organic fertilizers, natural P and Kfertilizers will be required for sustainable organic teaproduction in the long term.

ACKNOWLEDGMENTS

This work was supported by the National NaturalScience Foundation of China (Project No. 41171218,40771113), the Ministry of Science and Technology ofChina (No. 2011BAD01B02) and the Common Fundfor Commodities (No. CFC/FIGT/04). We appreciateProf PC Brookes in Rothamsted Research and Dr GVPangga in University of the Philippines for their mean-ingful comments and suggestions.

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