Accumulated Impacts of Sulfur Spraying on Soil Nutrient ...210.72.92.31/bitstream/353005/10134/1/Accumulated Impacts of Sulfur...Yuwu Li1,2 Yujie Xia3 Haiying Li4 Xiaobao Deng1 Liqing

Soil Air WaterCLEAN

CSAWAC 44 (8) 909-1084 (2016) · Vol. 44 · No. 8 · August 2016

www.clean-journal.com

Renewables

Sustainability

Environmental Monitoring

8 | 2016

Yuwu Li1,2

Yujie Xia3

Haiying Li4

Xiaobao Deng1

Liqing Sha1

Bing Li3

Luxiang Lin1

Min Cao1

1Key Laboratory of Tropical ForestEcology, Xishuangbanna TropicalBotanical Garden, Chinese Academyof Sciences, Yunnan, China

2Key Laboratory of Rubber Biologyand Genetic Resource Utilization,Ministry of Agriculture, Hainan, China

3Kunming Institute of Zoology,Chinese Academy of Sciences,Yunnan, China

4National Research Center forSustainable HydropowerDevelopment, China Institute ofWater Resources and HydropowerResearch, Beijing, China

Research Article

Accumulated Impacts of Sulfur Spraying on SoilNutrient Availability and Microbial Biomass inRubber Plantations

Sulfur spraying is a conventional prevention and control measure for rubber leafdiseases in the northernmargin of tropical Southeast Asia. The aim of this study was todetermine the long-term (48 years) accumulated effects of sulfur spraying on somemajor soil microbial and nutrient properties in the area of rubber plantation. Theresults indicate a significant decrease in pH along the rubber chronosequence withyearly sulfur application. A negative effect of sulfur spraying on soil total sulfur contentwas also observed. Apart from that, soil microbial characteristics increasedsignificantly, except for microbial biomass carbon. Soil nutrient bioavailability-relatedcharacteristics showed a complex pattern of response to sulfur spraying, among whichbio-available ammonium nitrogen increased linearly, bio-available nitrate nitrogenshowed a trend resembling a large resting capital letter “S”, bio-available phosphorusshowed a contrary trend to nitrogen, a capital letter “S” resting the other direction,whereas bio-available potassium had no response to sulfur spraying. Based on thecomprehensive response indexes, soil microbial characteristics had a pulsing responseto sulfur spraying accumulation and two critical turning points were sometimebetween the 23rd and 32nd year and between the 40th and 48th year. Soil nutrientbioavailability showed a volatile comprehensive pattern, but there was no significantdifference during the chronosequence. There is need for control sulfur depositionfrequency and dosage under the soil and environmental safety threshold in the diseasesprevention and control in monoculture rubber plantation.

Keywords: Monoculture rubber plantation; Risk assessment; Soil acidification; Soil microbialactivity; Sprayed sulfur deposition

Received: June 21, 2014; revised: June 16, 2015; accepted: April 8, 2016

DOI: 10.1002/clen.201400397

: Additional supporting information may be found in the online version of this article at thepublisher’s web-site.

1 Introduction

The rubber tree (Hevea brasiliensis) is the most important source ofnatural rubber for the manufacture of rubber products and latexcoagulates. According to the Food and Agriculture Organization ofthe United Nations, FAO, statistics, the world rubber plantation area

reached 10.06 million ha by 2010 [1]. The rubber tree is native to theAmazon region (Brazil, Bolivia, Ecuador, and Peru), was introducedto tropical regions of Asia [2], and nowadays 81% of the world’srubbers are planted in South Asia and Southeast Asia [1]. Indonesia,Malaysia, Thailand, and other countries form a very importantrubber belt. In addition to the traditional planting regions, therubber plantation region has expanded to the northern montanemainland area of Southeast Asia, especially in southwest China,Laos, Cambodia, Myanmar, northeast Thailand, and northwestVietnam. At present, the rubber plantations in these regions are intotal >1.5 million ha [3]. Xishuangbanna is an important typicalrubber-producing area in this northern margin of Southeast Asiatropics and has the highest unit yield of rubber latex in the world(http://news.xinhuanet.com/fortune/2004-08/31/content_1929540.htm) [4]. The rubber plantation area had reached approximately halfa million ha in Xishuangbana by 2010 [5].A large number of rubber plantation studies in the literature

focus on the impact of land use conversion on the properties anddynamics of soil nutrients, biology, structure and function [6, 7].

Correspondence: Dr. Y. Li, Key Laboratory of Tropical Forest Ecology,Xishuangbanna Tropical Botanical Garden, Chinese Academy ofSciences, Yunnan 650223, ChinaE-mail: [email protected]

Abbreviations: Bioavai-K, total bio-available potassium; Bioavai-N, totalbio-available nitrogen; Bioavai-P, total bio-available phosphorus; Bioavai-NH4

þ, bio-available ammonium nitrogen; Bioavai-NO3�, bio-available

nitrate nitrogen; CRI, soil comprehensive response index;DBH, diameterat breast height;DP, decay production period; FDA, fluorescein diacetate;HP, high production period; ICP-AES, inductively coupled plasmaatomic-emission spectrometry; IP, initial production period; NP, noproduction period; SMB, microbial biomass; SWC, soil water content;TMA, total microbial activity; TS, soil total sulfur.

1001

© 2016 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.clean-journal.com Clean – Soil, Air, Water 2016, 44 (8), 1001–1010

http://news.xinhuanet.com/fortune/2004-08/31/content_1929540.htm

http://news.xinhuanet.com/fortune/2004-08/31/content_1929540.htm

However, little research has been performed on the impact ofcurrent management measures on soil properties and dynamics.Powdery mildew and rubber anthracnose are two major tree leafdiseases in rubber plantations worldwide. There are many historicalreports about the adverse effects on rubber plantation managementand dry latex production with disease outbreaks in Malaysia, India,Brazil, and Papua New Guinea [8–10]. Considering the marginalregion for rubber plantations based on the environmentalconditions (low temperature in winter and a distinctive dryseason) [3], the northern region of Southeast Asia, especially insouthwest China, Laos, Cambodia, Myanmar, northeast Thailand,and northwest Vietnam, suffers more serious from invasion ofpowdery mildew and rubber anthracnose diseases.Powdery mildew is mainly caused by rubber powder spores

(Oidium heveae), which were first reported by Steinmann in 1925 [2].Rubber anthracnose is caused mainly by Colletotrichum gloeosporioidesor by C. acutatum [11, 12]. Sulfur spraying is a conventionalprevention and control practice for the powdery mildew andanthracnose diseases of rubber plantations. Because sulfur powderis the cheapest butmost effective pesticide, every year, farmers spraysulfur powder once or twice during the leaf-expansion period of therubber tree during February and March. The average spraying rate is15 kgha�1. Based on the previous rubber plantation area data, 6300–12 700 tons of sulfur powder is sprayed every year in rubberplantations in Xishuangbanna.Many studies have focused on the effects of sulfur on soil pH, the

solubility of heavy metals and the soil biogeochemistry process [13,14]. Application of sulfur either as a fertilizer or plant protectionagent was reported to decrease soil pH [15, 16]. Maynard et al. [17]reported the negative effect of sulfur on heterotrophs in forest soils.However, relatively few studies have focused on the depositioneffects of sulfur after being sprayed on the soil biogeochemicalproperties of monoculture rubber plantations. Could the practicecorrect soil sulfur deficiency or cause soil acidification, nutrientleaching and even other environmental hazards? This studyinvestigated the long-term (48 years) accumulated deposition effectsof sulfur spraying on soil biogeochemical properties of monoculturerubber plantations in Xishuangbanna, one of the most importantrepresentative rubber planting and management area of SoutheastAsia.

2 Materials and methods

2.1 Study site

The study was conducted in the Menglun rubber plantation area (21°550 N, 101°160 E), one of the most important rubber planting areas inXishuangbanna, Yunnan Province, Southwest China, near theXishuangbanna Tropical Botanical Garden, Chinese Academy ofSciences (XTBG, CAS) (Supporting Information Fig. S1). Located in thenorthern margin of Southeast Asia, Xishuangbanna is dominated bywarm-wet air masses from the Indian Ocean in summer andcontinentalairmassesfromthe temperateregions inwinter, resultingin a highly seasonal climate [18, 19]. The annualmean temperature is21.7°C, and the annual mean rainfall is 1512mm (1980–2008) [20].In this study, the approach of spatial sequence instead of temporal

sequence was used to reflect the dynamics of the rubber plantationecosystems. The experimental design consisted of nine forest-agesites of a monoculture rubber plantation as a plantation chronose-quence (1–48 years). The plantation ages were 1, 5, 8, 10, 15, 23, 32,

40, and 48 years. There were nine replicate plots within eachplantation site. All sites were located on yellow latosol developedfrom purple sandstone at elevations between 560 and 750m withthe same vegetation conversion history (tropical secondary forest torubber plantation by slash-and-burn and rubber planted process).And the slope aspects of the sites were similar (to south or westsouth). The maximum distance of each site was nomore than 10 km.The vegetation characteristics and management measures of therubber plantation at different plantation ages are given inSupporting Information Table S1. And the “annually weedingfrequency” means the time or frequency of cutting down oreradicating weeds under rubber plantations every year.

2.2 Soil sampling and analysis

Soil sampling was conducted during January 2013, at the end of therubber tree’s deciduous period. At each site, a 30� 30m2 survey plotwas established (four rows of rubber trees and three 10-m widehedgerows), containing nine sampling subplots, three at each slopeposition (up slope, middle slope, low slope) (Supporting InformationFig. S2) [20]. At each subplot, two composite soil samples (�500 g)were collected (avoiding fertilization holes and tree trunks of >3m)with a soil auger to a depth of 10 cm after the litter-fall and/or grasslayer was carefully removed. After removing any visible plant debrisincluding roots and stones, each soil sample was sieved with a 2-mmsieve and kept at 4°C; the biochemical analysis was carried outwithin two weeks. The other soil sample was dried at roomtemperature (�20°C) for approximately two weeks and then storedat room temperature in an air tight container for chemicalanalysis [20].Twelve soil variables from three functional subgroups were

chosen. The first subgroup includes soil total sulfur (TS) (HClO4/HFdigestion and inductively coupled plasma atomic-emission spec-trometry (ICP-AES), iCAP6300, Thermo Fisher Scientific, USA) [21].The second subgroup includes four microbial-related variables:microbial biomass sulfur (SMB-S) (fumigation-extraction and ICP-AES) [22, 23], microbial biomass carbon (SMB-C), microbial biomassnitrogen (SMB-N) (fumigation-extraction and total organic carbonanalysis, Vario MAX CN, Elementar Analysensysteme, Germany) [22,24], and soil total microbial activity (TMA) (fluorescein diacetatehydrolysis). Schn€urer and Rosswall [25] found that spectrophoto-metric determination of the hydrolysis of fluorescein diacetate (FDA)was a simple, sensitive, and rapidmethod for determiningmicrobialactivity in soil. The third subgroup includes five nutrientbioavailability-related variables: bio-available nitrogen (bioavai-N),bio-available ammonium-N (bioavai-NH4

þ), bio-available nitrate-N(bioavai-NO3

�), bio-available phosphorus (bioavai-P) and bio-avail-able potassium (bioavai-K) (Ion exchange resins method) [26, 27]. Inthis study, the soil nutrient bioavailability of N, P, and K wereestimated by the ion-exchange resin extraction method for it cansimulate the biological uptake functioning of plant roots [28–33].The final subgroup includes soil water content (time domainreflection method) and pH (pH-meter) (dry soil/deionized water,1:2.5)) [21]. The variables were measured according to the protocolsgiven in Supporting Information Table S2.

2.3 Soil comprehensive response index

Based on the percentage positions of soil property values betweenthe maximum and minimum during the study period (1–48 years),

1002 Y. Li et al.


the soil comprehensive response index (CRI) was used to estimate thecomprehensive response of the four chosen soil microbial-relatedproperties (SMB-S, SMB-C, SMB-N, and TMA) or the soil nutrientbioavailability (bioavai-NH4

þ, bioavai-NO3�, bioavai-P, and bioavai-K)

of the rubber plantation to the sulfur spraying along thechronosequence. CRI is given in Eq. (1), based on Supporting dataTable S3.

with i¼ 1, 2, 3, 4 and j¼ 1, 5, 8, 10, 15, 23, 32, 40, 48.where j is one of the total nine plantation age points; Vji is the value

of the ith soil microbial-related or nutrient bioavailability-relatedvariableof thefourchosenvariablesof the jthyear’s rubberplantation;Vi min is the minimum value of this property; Vi max is the maximumvalue of this property; n is the number of soil microbial-relatedor nutrient bioavailability-related variables (n¼ 4). R12 is the correla-tionvalueofSMB-SandSMB-CorTSandbioavai-N.R13 is thecorrelationvalue of SMB-S and SMB-N or TS and bioavai-P. R14 is the correlationvalueof SMB-S andTMAorTSandbioavai-K.R23 is the correlation valueof SMB-C and SMB-N or bioavai-N and bioavai-P. R24 is the correlationvalue of SMB-C and TMA or bioavai-N and bioavai-K. R34 is thecorrelation value of SMB-N and TMA or bioavai-P and bioavai-K.

2.4 Data analysis

For the analyses, every site had nine replicates (N¼ 9). Pearsoncorrelation was used to assess the correlation among soil propertiesacross all sites. Least significant difference, LSD, was used to assesspair wise differences (at 5% level). Statistical analyses wereconducted using the package SPSS 13.0 (SPSS, Chicago, IL, USA).

3 Results

3.1 Soil pH and soil water content

The range of soil pH values was from 4.41 to 5.61 during the 48 yearsin the studied rubber plantations, and the average value was 4.85(Fig. 1, Table 1). A significant correlation was found between soil pHand plantation ages (R2¼ 0.674, P¼ 0.000) (Fig. 1). Soil pH had alogarithmic decreasing trend along the rubber plantation chro-nosequence (1–48 years), the maximum value appeared the first yearafter the rubber trees were planted (pH 5.61), and the soil pH hastended to be stable until 23 years (pH 4.58) (Table 1).The range of soil water content (SWC) contents was from 19.26% to

39.16% during 48 years within the studied rubber plantation, andthe average value was 27.32� 0.85% (Fig. 1, Table 1).

3.2 Soil total sulfur content

In the present experiment, the TS content ranged from 103.89 to150.89mgkg�1 during the rubber plantation chronosequence

(1–48 years), and the average value was 123.10� 2.33mgkg�1

(Table 1). Significant correlation was found between soil TS andplantation ages (R2¼0.332, P¼0.000) (Fig. 2). Soil TS had neither alinear decreasing nor a linear increasing relationship with theaccumulated sulfur application along the rubber plantationchronosequence, and the change followed a power function withplantation age. The maximum value appeared during the year the

rubber trees were planted (TS1 yr¼ 150.89� 4.77mgkg�1) (Table 1),and then the soil TS had a decreasing trend during the “noproduction period” (NP) and “initial production period” (IP) fromone to 15 years (TS15 yr¼ 104.11� 2.04mgkg�1) (Table 1). During the“high production period” (HP), soil TS increased slowly with thesprayed sulfur accumulation. However, when the rubber treesentered the older ages and the “decay production period” (DP), soilTS rapidly decreased to the minimum value in the 48th year(TS48 yr¼ 103.89� 3.16mgkg�1) (Fig. 2, Table 1).

y = -0.3285Ln(x) + 5.6815R2 = 0.6743P =0.000

4.04.24.44.64.85.05.25.45.65.86.0

0 10 20 30 40 50

Rubber plantation age (years)

Soi

l pH

R2 = 0.0793P=0.094>0.05

0

10

20

30

40

50

60

70

0 10 20 30 40 50


SWC

(%)

Figure 1. The relationship of soil pH and soil water content with yearlysulfur application along the rubber plantation chronosequence. The blackline is the regression curve.

CRIj ¼ 1n�Xni¼1

Vji � Vi min

Vi max � Vi min� 100% ¼ 1

4�

Vj1 � V1 min

V1 max � V1 minþ

Vj2 � V2 min

V2 max � V2 min

� �� 1� R12ð Þþ

Vj3 � V3 min

V3 max � V3 min

� �� 1� R13 � R23 � 1� R13ð Þ½ �þ

Vj4 � V4 min

V4 max � V4 min

� �� 1� R14 � R24 � 1� R12ð Þ � R34 � 1� R13 � R23 � 1� R12ð Þ½ �f g

8>>>>>>>>>>>><>>>>>>>>>>>>:

9>>>>>>>>>>>>=>>>>>>>>>>>>;

� 100%

ð1Þ

Soil 1003


Tab

le1.

Soilp

rope

rtych

ange

swith

sulfu

rsp

raye

dev

eryye

aralon

gtherubb

erplan

tatio

nch

rono

sequ

ence

(Mea

n�SE,n¼9)

Rubb

erplantation

chronoseq

uen

ce(year)

Soilvariab

le1

58

1015

2332

4048

Average

Totalsu

lfur

content

TS(m

gkg

�1)

150.89

�4.77

112.56

�1.79

150.11

�7.86

104.89

�1.31

114.11

�2.04

109.89

�3.66

136.44

�4.99

125.00

�2.11

103.89

�3.16

123.10

�2.33

Microbial-related

SMB-S

(mgkg

�1)

0.97

�0.22

0.55

�0.12

0.52

�0.10

0.50

�0.12

1.18

�0.15

0.91

�0.11

1.89

�0.29

2.42

�0.21

0.66

�0.12

1.07

�0.09

SMB-C

(mgkg

�1)

87.98�25

.97

84.80�10

.76

99.71�24

.68

75.94�19

.40

55.90�12

.45

101.01

�27

.03

135.28

�25

.00

113.99

�32

.40

85.93�16

.29

93.39�7.54

SMB-N

(mgkg

�1)

10.62�1.68

10.14�1.40

9.66

�1.35

9.90

�0.99

11.48�1.45

12.23�1.22

20.47�2.28

18.20�1.41

9.58

�1.43

12.48�0.64

TMA(mgFD

Akg

�1h�1)

75.65�2.70

97.19�2.28

55.96�4.17

94.01�2.43

94.46�2.72

71.71�7.96

87.83�2.97

92.23�3.83

91.98�3.74

84.56�1.93

Nutrient

bioa

vailab

ility-

related

Bioavai-N

(mgkg

�1)

9.97

�0.83

10.52�0.45

6.88

�0.62

9.80

�0.38

10.75�0.58

8.98

�0.66

11.93�0.89

12.22�1.08

9.93

�0.64

10.11�0.30

Bioavai-NH4þ

(mgkg

�1)

7.10

�0.31

7.54

�0.54

6.22

�0.60

8.94

�0.31

9.26

�0.55

7.48

�0.63

8.60

�0.57

10.30�1.01

8.00

�0.58

8.16

�0.24

Bioavai-NO3-

(mgkg

�1)

2.86

�0.58

2.98

�0.47

0.65

�0.06

0.86

�0.13

1.49

�0.13

1.50

�0.27

3.33

�0.46

1.92

�0.26

1.93

�0.33

1.95

�0.16

Bioavai-P

(mgkg

�1)

1.35

�0.11

2.86

�0.50

4.24

�0.84

1.23

�0.12

1.50

�0.15

1.26

�0.23

1.36

�0.10

2.14

�0.19

3.43

�0.54

2.15

�0.19

Bioavai-K

(mg

kg-�

1)

43.5�54

.62

62.64�11

.48

45.87�3.62

62.33�8.01

53.37�2.13

42.81�2.62

57.33�13

.80

49.83�1.08

36.49�4.44

50.47�2.48

Others

pH

5.61

�0.10

4.90

�0.07

5.53

�0.11

4.97

�0.07

4.75

�0.04

4.58

�0.10

4.45

�0.05

4.43

�0.02

4.41

�0.05

4.85

�0.06

SWC(%)

22.91�0.51

34.70�1.12

25.81�1.69

27.36�1.12

29.25�1.46

19.26�2.55

39.16�3.12

25.55�0.88

21.88�0.91

27.32�0.85

1004 Y. Li et al.


3.3 Soil microbial-related properties

3.3.1 Soil microbial biomass sulfur

The range of SMB-S content was from 0.50 to 2.42mgkg�1 during the48 years in the studied rubber plantation, and the average value was1.07� 0.09mgkg�1 (Table 1). SMB-S has a significant relationship withrubber plantation age (R2¼ 0.169, P¼ 0.000) (Fig. 3). Soil SMB-S increasedlinearly along the rubber plantation chronosequence with the sprayedsulfur accumulation. During the first decade (“NP period” and the early“IP period”), SMB-S was at a minimum (average value of 0.64� 0.07mgkg�1) (Table1)andthenincreasedduringthethreefollowingperiods (thelate “TP period”, the “HP period”, and the first half of the “DP period”),until it reached the maximum value in the 40th year (2.42� 0.21mgkg�1) (Fig. 3, Table 1). However, during the late “DP period”, SMB-Sdecreasedrapidly fromthemaximumvalue inthe40thyear tothe initialstage level in the 48th year (0.66�0.12mgkg�1) (Fig. 3, Table 1).

3.3.2 Soil microbial biomass carbon

The range of the SMB-C content was from 55.90 to 135.28mgkg�1

during the 48 years in the studied rubber plantation, and theaverage value was 93.39� 7.54mgkg�1 (Table 1). No significantcorrelation was found between SMB-C and rubber plantation age(R2¼ 0.065, P¼ 0.155) (Fig. 3).

3.3.3 Soil microbial biomass nitrogen

The range of the SMB-N content was from 9.58 to 20.47mgkg�1

during the 48 years in the studied rubber plantation, and theaverage value was 12.48� 0.64mgkg�1 (Table 1). SMB-N also had asignificant relationship with rubber plantation age (R2¼ 0.108,P¼0.003) (Fig. 3). Similarly with the dynamic pattern of SMB-S, soilSMB-N increased linearly along the rubber plantation chronose-quence. During the “NP period” and the early “IP period”, SMB-Nshowed also a minimum (average value of 10.08� 0.66mgkg�1)(Fig. 3), and then the SMB-S increased during two different periods(the late “TP period” and “HP period”). However, themaximum value(20.47� 2.28mgkg�1) appeared at the end of the “HP period” (in the32nd year), eight years earlier compared with SMB-S. During thewhole “DP period”, SMB-S showed a decreasing trend from the 32ndto the 48th year, and the value in the 48th year was lower than theinitial stage level (9.58� 1.43mgkg�1) (Fig. 3, Table 1).

3.3.4 Soil total microbial activity

The range of the soil TMA content was from 55.96 to 97.19mg kg�1

h�1 during the 48 years in the studied rubber plantation, and theaverage value was 84.56� 1.93mg kg�1 h�1 (Table 1). A significantcorrelation was found between TMA and rubber plantation age(R2¼ 0.050, P¼ 0.046) (Fig. 3), but the slope of the linear equationwasvery small (k¼ 0.274) (Fig. 3), as the accumulated changes of the48 years were 15.6% of the average TMA value (0.274� 48/84.56¼ 15.6%) (Fig. 3, Table 1).

3.4 Soil bioavailability-related properties

3.4.1 Soil bio-available nitrogen

Soil bioavai-N was the sum of the soil bioavai-NH4þ and bioavai-NO3

-,and ranged from 6.88 to 12.22mgkg�1 during the 48 years in thestudied rubber plantation, and the average value was 10.11� 0.30mgkg�1 (Table 1). It was significantly correlated with rubber treematurity (R2¼ 0.209, P¼ 0.008) (Fig. 4), following a power functionwith the minimum value at the beginning year of the rubber latexharvest (eighth year) (6.88� 0.62mgkg�1) and the maximum valueat the middle “DP period” (�40th year) (12.22� 1.08mgkg�1). At theend of the “DP period” (48th year), it returned to the level of theinitial stage (first year), 9.97� 0.83 and 9.93� 0.64mgkg�1,respectively (Fig. 4, Table 1).Soil total bioavai-NH4

þ ranged from 6.22 to 10.30mgkg�1, and theaverage value was 8.16�0.24mgkg�1 (Table 1). Soil total bioavai-NO3

� ranged from 0.65 to 3.33mgkg�1, and the average value was1.95� 0.16mgkg�1 (Table 1). Soil bio-available NH4

þ and NO3-

accounted for 80.7 and 19.3% of the total bioavai-N, respectively.However, their variation patterns were very different along therubber plantation chronosequence. Soil bioavai-NH4

þ had a linearincreasing trend (R2¼ 0.105, P¼ 0.017), whereas soil bioavai-NO3

�

had a cubic change trend resembling a lying capital letter “S” (Fig. 4,Table 1).

3.4.2 Soil bio-available phosphorus

The range of the soil total bioavai-P content was from 1.23 to4.24mgkg�1 during the 48 years in the studied rubber plantation,and the average value was 2.15� 0.19mgkg�1 (Table 1). Soil totalbioavai-P had a significant cubic relationship with rubber plantationage (R2¼ 0.218, P¼ 0.006) (Fig. 4), but unlike the soil bioavai-N andbioavai-NO3

–, the bioavai-P showed an opposite trend resembling alying capital letter “S” (R2¼ 0.295, P¼ 0.001) (Fig. 4, Table 1).

3.4.3 Soil bio-available potassium

The range of the soil bioavai-K content was from 36.49 to62.64mgkg�1 during 48 years in these studied rubber plantations,and the average value was 50.47� 2.48mgkg�1 (Table 1). There wasno significant correlation between bioavai-K and rubber plantationage (R2¼ 0.068, P¼ 0.316) (Fig. 4).

4 Discussion

Non-timber forest crops take an important position in the economicdevelopment within the impoverished mountainous area ofSouthwestern China. The rubber tree is one of these types of forestcrops. This crop has also greatly improved local farmers’ living

y = -0.004 x3 + 0.304 x2 - 6.473 x + 155.065R2 = 0.332P =0.000

020406080

100120140160180200

0 10 20 30 40 50


Soi

l tot

al s

ulfu

r (m

g kg

-1)

Figure 2. The relationship between soil total sulfur content and the rubberplantation chronosequence with yearly sulfur application. The black line isthe regression curve.

Soil 1005


standard by harvesting the rubber latex and earning approximatelyRMB ¥75 000 ha�1 per year in Xishuangbanna [20]. The large area ofmonoculture plantations is subject to the occurrence of forest cropdiseases and insect pests. Sulfur spraying is the cheapest but mosteffective method for preventing and controlling rubber leafpowdery mildew and anthracnose. This study focused on thelong-term (48 years) accumulated effects of sulfur spraying on thesoil properties of monoculture rubber plantations.Application of sulfur either as a fertilizer or for plant protection

has been reported during the early 20th century to decrease soilpH [15, 16]. This phenomenon was repeatedly tested by short-termtime-scale studies on forest soil and agriculture soil in differentregions (e.g., [17, 34–36]). In this study, soil has a significant tendencytoward acidificationwith sprayed sulfur accumulation in the rubberplantation system when the plantation age was less than 30 yearsand that the soil acidity then remained stable in the later plantationages in this studied chronosequence. The reason for soil pHreduction was the large quantities of sulfur being oxidized to sulfateand releasing Hþ [14, 35, 37, 38].With the sprayed sulfur accumulation along the rubber planta-

tion chronosequence, the variation patterns of soil TS and soilmicrobial-related properties were distinct in Xishuangbanna (Figs. 2and 3, Table 1). Soil TS had neither a linear decreasing nor a linear

increasing relationship with the accumulated sulfur applicationalong the rubber plantation chronosequence, and the changefollowed a power function with plantation age. The extension of Ssprayed years also did not result in a cumulative increase of SMB-Cbut in a linear and continuous increase in SMB-S and SMB-N in thisstudy, especially during years 1 to 40 (P¼ 0.000). That is, sulfurspraying lowered the microbial biomass nutrient ratios, and sulfuraccumulation in the soil microbial biomass did not cause sulfuraccumulation within the soil. The reason was most likely either thatthe average ratio of SMB-S to soil total sulfur in rubber plantationsoil was too low (average ratio of SMB-S to TS, 1.38%) or that thesulfur was an active element in biogeochemical cycling (e.g., beingeasily oxidized or migrated and transformed). Wang et al. [34]reported that sulfur could significantly affect the soil microorgan-ism community composition after 31 days of incubation. Guptaet al. [36] reported that SMB-C had no significant response to a sulfuraddition of 22 kg ha�1 per year but increased significantly by 77% bydoubling the sulfur addition (44 kg ha�1 per year). Thus, thefollowing three possible reasons might explain the results. First,there were most likely some specific microorganisms, such asacidophilic bacteria, in the soil that can use sulfur as an energysource and oxidize sulfur to SO4

2� when the soil pH has decreased.These reactions may be catalyzed mainly by microbes [34, 39, 40].

y = 0.021x + 0.641R² = 0.169P =0.000

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

0 10 20 30 40 50


SM

B-S

(mg

kg-1

)

R2 = 0.065P =0.155>0.05

0

50

100

150

200

250

300

350

400

0 10 20 30 40 50


SMB-

C (m

g kg

-1)

y = 0.1202x + 10.045R2 = 0.1081P =0.003

0

5

10

15

20

25

30

35

40

0 10 20 30 40 50


SM

B-N

(mg

kg-1

)

y = 0.247 x + 79.567R2 = 0.050

P=0.046<0.05

0

20

40

60

80

100

120

0 10 20 30 40 50


Soi

l tot

al a

ctiv

ity (u

g FD

A k

g-1

h-1)

Figure 3. The relationship between soil microbial-related properties (SMB-S, SMB-C, SMB-N, and total microbial activity) and the rubber plantationchronosequence with yearly sulfur application. The black line is the regression curve.

1006 Y. Li et al.


Second, the abundance of soil bacterial groups may be shifted,especially some microbes that could not tolerate an acidicenvironment [36, 41]. The third reason was most likely that thecurrent sulfur spraying dose (15–18 kg ha�1 per year) did not reachthe threshold value of microbial populations but reached thethreshold value of changing the nutrient transformation status ofthe soil microbes.Alexander [42] reported that soil acidification reduced microbial

activity. Maynard et al. [17] reported the negative effects of sulfur

deposition on microbial activity in forest soils. However, informa-tion on the effects of long-term sulfur application on soil microbialactivity is lacking. In this study, soil total microbial activity was notdecreasing but increased slowly and showed a linear correlationalong the rubber plantation chronosequence (R2¼ 0.050, P¼ 0.046)(Fig. 3). However, this correlation was not significant, as the P-valuewas nearly 0.05 and the slope of the linear equation was very small(k¼ 0.274) (Fig. 3). The accumulative growth of the entire 48 yearswas only 15.6% of the average TMA value (Table 1). Soil total

y = -0.0003x3 + 0.0208x2 - 0.3288x + 10.523R2 = 0.209P=0.008

0

5

10

15

20

25

0 10 20 30 40 50


Soil

tota

l bio

avai

labl

e N

(mg

kg-1

)

y = 0.037 x + 7.414R2 = 0.105P=0.017

0

2

4

6

8

10

12

14

16

0 10 20 30 40 50


Soi

l bio

avai

labl

e N

H4+ (m

g kg

-1)

y = -0.0002x3 + 0.0183x2 - 0.3712x + 3.3894R2 = 0.2954P =0.001

0

1

2

3

4

5

6

7

0 10 20 30 40 50


Soil

bioa

vaila

ble

NO

3- (mg

kg-1

)

y = 0.0002x3 - 0.0094x2 + 0.1097x + 1.9989R2 = 0.2175P =0.006

0

1234

5678

9

0 10 20 30 40 50


Soil

bioa

vaila

ble

P (m

g kg

-1)

R2 = 0.068P = 0.316

0

20

40

60

80

100

120

140

0 10 20 30 40 50


Soi

l bio

avai

labl

e K

(mg

kg-1

)

Figure 4. The relationship between soil nutrient bioavailability-related properties (Bioavai-N, Bioavai-NH4þ, Bioavai-NO3

-, Bioavai-P and Bioavai-K) andthe rubber plantation chronosequence with yearly sulfur application. The black line is the regression curve.

Soil 1007


microbial activity remained at relatively high levels in the rubberplantation along the studied chronosequence in Xishuangbanna.From the complex responses of different soil microbial-related or

bioavailable nutrient-related properties in this study, it was verydifficult to assess the effect of sulfur spraying to soil ecosystems inmonoculture rubber plantation, using only one or two soilproperties as indicator, so the soil CRI was used to evaluate thecomprehensive response of soil microbial-related properties or soilnutrient bioavailability in this study. After eliminating thecorrelation between indicators, CRImicrobial showed the comprehen-sive response of soil microbial-related properties along thechronosequence in the rubber plantation. From the first to the23rd year, CRImicrobial was relatively stable and low, only 82.7% ofthe total average CRI value (23.7/28.7¼ 82.7%) (Fig. 5, Table 2), andthere was no significant difference during this period. This findingindicated that S-spraying did not significantly change the soilmicrobial community composition and function. However, whenthe rubber trees entered the end stage of the “HP period” andthroughout the whole “DP period” (32nd to 40th year), CRImicrobial

showed a significant increase (nearly one time) ((45.3–23.7)/23.7¼ 91.7%) (Fig. 5, Table 2). Thus, the response process of soilmicrobes to sulfur-accumulated spraying was possibly not a stableand linearly cumulative pattern but a pulsating pattern and that thetwo turning points were sometime between the 23rd and 32nd yearand between the 40th and 48th year (Fig. 5, Table 2).Plant growth and productivity depend considerably on the

availability of nutrients at the soil-root interface. Nutrientbioavailability is one of the important factors affecting thebiological nutrients uptake by plants and microorganisms in soilecosystems and is limiting the recovery rate of disturbedvegetation [43, 44]. In addition to the nutritional status, the plantrhizodeposition activity and soil microbiome along the plantslifespan are also important factors influencing nutrient bioavail-ability [45]. Soil rhizosphere microbial communities like mycor-rhizal fungi and rhizobacteria mineralize soil organic matter byreleasing hydrolytic enzymes and thus enhancing the nutrientavailability in soil [28, 29]. Several bacterial species have beencharacterized as P-solubilizing microorganisms (genera Azospir-illum, Azotobacter, Bacillus, Burkholderia, Pseudomonas, Rhizobium, andSerratia) [30–32, 45] while other species have been shown toincrease the solubility of micronutrients. The enhanced amount of

R2 = 0.7604(microbial)

R2 = 0.5261(biavailability)

10.0

20.0

30.0

40.0

50.0

60.0

70.0

0 5 10 15 20 25 30 35 40 45 50


CR

I (%

)

CRI(microbial)CRI(bioavailability)

Figure 5. The variation of the CRI indexes of soil microbial-relatedproperties (blue) and soil nutrient bioavailability (red) along the rubberplantation chronosequence with yearly sulfur application. T

able

2.The

percen

tage

positio

nan

dCRIof

soilmicrobial-related

prop

ertie

san

dnu

trient

bioa

vailabilitywith

sulfu

rsp

raye

dev

eryye

aralon

gtherubb

erplan

tatio

nch

rono

sequ

ence

(Mea

n,n¼9;

Mea

n�SE,n¼4)

Rubb

erplantation

chronoseq

uen

ce(year)

Soilvariab

lepercentage

andCRI

15

810

1523

3240

48

Microbial-related

SMB-S

(%)

28.75

12.32

11.05

10.31

37.05

26.21

64.83

85.67

16.47

SMB-C

(%)

35.35

34.45

40.94

30.60

21.88

41.51

56.41

47.15

34.94

SMB-N

(%)

20.71

18.45

16.22

17.35

24.71

28.20

66.54

55.98

15.86

TMA(%)

52.77

85.02

23.29

80.26

80.94

46.87

71.00

77.59

77.22

CRImicrobial

(%)

24.25�8.33

25.70�1.87

15.15�4.29

23.59�4.54

29.36�1.72

24.10�5.75

43.20�6.62

47.32�8.15

25.23�1.25

Nutrientbioa

vailab

ility-related

Bioavai-NH4þ(%)

77.78

23.81

76.19

9.52

25.40

19.05

58.73

41.27

12.70

Bioavai-NO3�(%)

49.34

45.59

24.07

42.10

49.44

39.04

63.66

65.36

49.81

Bioavai-P

(%)

21.45

42.62

60.53

30.75

22.35

22.50

21.55

33.74

44.96

Bioavai-K

(%)

16.89

35.58

31.80

38.68

35.35

24.62

40.92

35.71

29.87

CRIbioa

vailab

ility(%)

41.69�4.89

38.24�6.65

52.69�13

.53

29.72�10

.97

31.67�6.23

26.15�5.92

43.81�8.92

43.80�6.41

36.52�5.68

1008 Y. Li et al.


soluble macro- and micronutrients in the close proximity of thesoil-root interface has indeed a positive effect on plant nutrition. Inthis context, the quality and biological activities of both roots andmicroorganisms play an important role in rubber plantationnutrient availabilities [33, 45]. Estimating nutrient availability (e.g.,available phosphorous) in forest soils is difficult because of highspatial variability, seasonal fluctuation of nutrient pools, and theproblems associated with distinguishing between available andnon-available nutrient fractions [46]. The ion-exchange resinextraction method was used to estimate the soil nutrientbioavailability of N, P, and K by simulating the uptake functioningof plant roots [26, 27, 47–50].Wang et al. [34] found that S could facilitate the plants’ uptake of

some cations, such as Cu2þ and Zn2þ. In the present study, soilexchangeable NH4

þ showed an increasing trend along theplantation chronosequence or with S-spraying (Fig. 4), but theother three chosen variables of soil nutrient bioavailability showedvery different response patterns, among which bioavai-NO3

– was alarge lying capital letter “S”(8 ) (Fig. 4) and bioavai-P was anopposite-lying capital letter “S” (�) (Fig. 4), whereas bioavai-K hadno response to S-spraying along the chronosequence within therubber plantation (Fig. 4). This result indicates that soil bioavai-Kdid not vary with the accumulation of sprayed sulfur along therubber plantation chronosequence. There was no bio-availablenutrient variable decrease along the first eight years but a sharpincrease at eight to nine years (N, P, K fertilization start afterrubber tree planted eight years), which may have some relationshipwith fertilization methods of rubber plantation. Holes or furrowsfertilizationmethods were used near the rubber trees (�20 cm deepholes or furrows in the soil surface with a pointed implement,0.5� 1.0m away from the tree trunk) in the field. Moreover,possibly different soil bio-available nutrient variables had theirown response and feedback to the same environmental stress ormanagement within the rubber plantation. The responses andfeedbacks of different soil bio-available nutrient variables weredifferent to the S spraying, which may be due to the soil’s strongbuffer capacity. Previous studies have shown that soil acidificationwould lead to some changes in the solubility of organic matterwith sulfur and other acidic substances applied during the processof agriculture or forestry production and management [51], andsuch changes might influence the leaching of organic matter (e.g.,lowmolecular weight organics) from the biologically active surfacehorizons [52].CRIbioavailability showed the comprehensive response of soil

nutrient bioavailability along the chronosequence within therubber plantation (Fig. 5, Table 2). CRIbioavailability showed a volatilitypattern (1st% 8th↘ 23rd% 32nd! 40th↘48th), but there were nosignificant differences in the different tree ages except the eighthand 23rd year. The CRIbioavailability pattern was different from theCRImicrobial pattern. Especially in the NP and IP periods (�15 years),the patterns of CRIbioavailability and CRImicrobial were opposite. It istherefore suggested that there may be no response process of soilnutrient bioavailability to sulfur accumulated spraying in thenorthern margin of Southeast Asia.Sulfur powder spraying is the cheapest measure for the

prevention and control of rubber leaf powdery mildew andanthracnose, but there is need for control the depositionfrequency and dosage under the soil and environmental safetythreshold and minimize its risk in monoculture rubber planta-tion management.

Acknowledgments

This study was supported by the Project of the Natural ScienceFoundation of China (NSFC41201298), the Strategic PriorityResearch Program of the Chinese Academy of Sciences(XDA05070303), the Opening Project Fund of Key Laboratory ofRubber Biology and Genetic Resource Utilization, Ministry ofAgriculture of China (RRI-KLOF1407), and the Opening Project Fundof Key Laboratory of Tropical Forest Ecology, Chinese Academy ofSciences (09KF001B04). We thank staff members of XishuangbannaStation for Tropical Rainforest Ecosystem Studies for their assistancein the field work and Biogeochemistry Lab of XishuangbannaTropical Botanical Garden, Chinese Academy of Sciences for soilanalysis. We are also grateful to Dr. Chao Shang, Crop and SoilEnvironmental Science Department, Virginia Polytechnic Instituteand State University for his valuable comments and Elsevier, UK, forits English language editing services on the manuscript. Finally, wewould like to convey our deepest gratitude to the anonymousreviewers, the Editors for their valuable comments which supportedus to develop the manuscript.

The authors have declared no conflict of interest.

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1010 Y. Li et al.


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Accumulated Impacts of Sulfur Spraying on Soil Nutrient ...210.72.92.31/bitstream/353005/10134/1/Accumulated Impacts of Sulfur...Yuwu Li1,2 Yujie Xia3 Haiying Li4 Xiaobao Deng1 Liqing