REGULAR ARTICLE

Occluded C in rice phytoliths: implications to biogeochemicalcarbon sequestration

Zimin Li & Zhaoliang Song & Jeffrey F. Parr &

Hailong Wang

Received: 17 October 2012 /Accepted: 25 February 2013# Springer Science+Business Media Dordrecht 2013

AbstractAims Carbon (C) bio-sequestration within the phytolithsof plants, a mechanism of long-term biogeochemical Csequestration, may play a major role in the global C cycleand climate change. In this study, we explored the poten-tial of C bio-sequestration within phytoliths produced incultivated rice (Oryza sativa), a well known siliconaccumulator.Methods The rice phytolith extraction was undertakenwith microwave digestion procedures and the determi-nation of occluded C in phytoliths was based ondissolution methods of phytolith-Si.Results Chemical analysis indicates that the phytolith-occluded C (PhytOC) contents of the different organs

(leaf, stem, sheath and grains) on a dry weight basis in 5rice cultivars range from 0.4 mgg−1 to 2.8 mgg−1, and theC content of phytoliths from grains is much lower thanthat of leaf, stem and sheath. The data also show that thePhytOC content of rice depends on both the content ofphytoliths and the efficiency of C occlusion withinphytoliths during rice growth. The biogeochemical Csequestration flux of phytoliths in 5 rice cultivars is ap-proximately 0.03–0.13 Mg of carbon dioxide (CO2)equivalents (Mg-e-CO2) ha

−1year−1. From 1950 to 2010,about 2.37×108Mg of CO2 equivalents might have beensequestratedwithin the rice phytoliths in China. Assuminga maximum phytoliths C bio-sequestration flux of0.13 Mg-e-CO2 ha−1year−1, the global annual potential

Plant SoilDOI 10.1007/s11104-013-1661-9

Responsible Editor: Hans Lambers.

Z. Li : Z. Song (*) :H. WangSchool of Environmental and Resource Sciences,Zhejiang A & F University, No. 88 North Huancheng Road,Lin’an, Zhejiang 311300, Chinae-mail: songzhaoliang78@163.com

Z. Song :H. WangZhejiang Provincial Key Laboratory of CarbonCycling in Forest Ecosystems and CarbonSequestration, Zhejiang A & F University,Lin’an, Zhejiang 311300, China

Z. SongLaboratory for Earth Surface Processes,Ministry of Education, Peking 100871, China

Z. SongCollege of Urban and EnvironmentalSciences, Peking University,Peking 100871, China

J. F. ParrSouthern Cross GeoScience,Southern Cross University, Lismore,NSW 2480, Australia

rate of CO2 sequestrated in rice phytoliths would approx-imately be 1.94×107Mg.Conclusions Therefore rice crops may play a signifi-cant role in long-term C sequestration through theformation of PhytOC.

Keywords Carbon sequestration . PhytOC .

Phytolith . Rice

Introduction

Climate change is one of the major global environ-mental issues (Schlesinger 1997). Increased green-house gas (GHG) emissions are now widely acceptedas the main cause of climate change since theIndustrial Revolution (Schimel 1995; Falkowski etal. 2000; IPCC 2007; Kosten et al. 2010). Recentresearch indicates that the global CO2 emission ratehad increased to 3.11×1011Mg per year by 2010(DOE 2008). With this in mind all mechanisms ofcarbon (C) sequestration should be explored in orderto identify relevant practical measures that may betaken to reduce the concentration of CO2 in atmo-sphere (Parr et al. 2010). Existing forestry, grasslands,shrub lands and wetland plants play a key role in thesequestration of atmospheric CO2. A large part of theC sequestrated by plants is returned into the soil asplant residues (Harrison et al. 1993; Parr and Sullivan2005; Fang et al. 2007; Field 2001). It is estimated thatsoils contain about 1550 Pg inorganic C and 950 Pgorganic C (Zuo and Lü 2011). A minor variation insuch big C pool in terrestrial ecosystems may have asignificant effect on the C flux (Harrison et al. 1993).However, due to environmental complexities, it isdifficult to quantify soil C changes (McKenzie et al.2000; Skjemstad et al. 2000; Clark 2002).

Phytoliths, the opaline amorphous silica formed inplant tissues (e.g., cell walls, cell lumina, and intercellularspaces typically near evaporating surfaces), are present inmost plants (Perry et al. 1987; Piperno 1988; Song et al.2012a, b). When plants die and undergo decomposition,large amounts of these phytoliths are released directlyinto the soil. When phytoliths encounter someunpredictable situations, such as earthquake, dust storms,flood (Baker et al. 1961), forest/grassland fire, erosion,etc., they are often preserved in the environment (Baker1961; Jones and Milne 1963; Wilding et al. 1967; Jonesand Handreck 1967; Wilding and Drees 1974; Sangster

and Parry 1981; Pearsall 1989; Hart and Humphreys1997; Parr 2006; Bowdery 2007). For example, it hasbeen reported that phytoliths in volcanic soils andpeatland sediments range in age from 0 to 8,000 yearBP (Parr and Sullivan 2005). Wilding (1967) reported aradiocarbon date of 13300±450 year BP for phytoliths.

During the formation of phytoliths, some organic Ccan be occluded (Jones and Milne 1963). Comparedwith other organic C fractions, phytolith occluded C(PhytOC) is relatively stable and can persist in the soilfor millennia due to its strong resistance to decompo-sition (Wilding et al. 1967; Wilding and Drees 1974;Mulholland and Prior 1993; Strömberg 2004; Parr andSullivan 2005; Prasad et al. 2005). PhytOC plays amajor role in soil C cycle (Parr and Sullivan 2005;Oldenburg et al. 2008) and the importance of the soilC cycle in relation to climate change has been empha-sized by many researchers (Gifford 1994; Falkowskiet al. 2000; Kosten et al. 2010). As an important partof terrestrial C, it can represent up to 82 % of total C insome soil and sediments after 2,000 years of litter leafdecomposition (Parr and Sullivan 2005). Recent re-search also indicates that plant phytoliths have greatpotential to sequester CO2 from the atmosphere (Parret al. 2009; Parr et al. 2010; Parr and Sullivan 2011;Zuo and Lü 2011). For example, the phytolith C bio-sequestration fluxes from millet, wheat and sugarcanerange up to 0.04, 0.25 and 0.36 Mg-e-CO2 ha

−1year−1,respectively (Parr et al. 2009; Parr and Sullivan 2011;Zuo and Lü 2011). Moreover, the flux of C occludedwithin the phytoliths of bamboo species examined todate ranges up to 0.71 Mg-e-CO2 ha−1year−1, and,with current global bamboo forests covering an areaof around 22 million ha could potentially be securelysequestering~1.56×107Mg of atmospheric CO2 peryear. Parr et al. (2010), have suggested that if allpotentially arable land (4.1 billion ha) is exploited togrow bamboo or other similar grass crops, the globalpotential of phytolith C bio-sequestration is approxi-mately 1.5×109Mg CO2 per year. This would result ineffectively reducing global CO2 emissions by a rateequivalent to 11 % of the current increased CO2 inatmosphere (Parr et al. 2010).

Cultivated rice (Oryza sativa) is a main food source formore that 50 % of the global population and is currentlycultivated on around 1.55×108ha (IRRI 2011). China isthe largest country involved in rice production, accountingfor up to 35 % of all world production, followed by India(22 %), Indonesia (9 %) and Bangladesh (7 %) (IRRI

Plant Soil

2011). There is a long history of rice production inChina (Cao et al. 2007) and its current area of produc-tion is around 2.96×107ha (NBSC 2011). Rice is able tobe cultivated twice per year under the high temperatureand abundant rainfall environment of south-easternChina (Cao and Zhang 2004; Lin et al. 2004).Recently the C sequestration potential of phytolithswithin crops of millet (Zuo and Lü 2011) and wheat(Parr and Sullivan 2011) has been reported. However,the variability of PhytOC in rice has not been investi-gated yet, even though cultivated rice is a well knownsilica accumulator (Epstein 1994, 1999). Therefore, theobjective of this study is to explore the potential of Coccluded within phytoliths in rice cultivars.

Materials and methods

Collection of rice plant materials

In this study, the rice plants used in experiment weregrown under the same conditions to eliminate factorsthat might influence silica uptake and deposition. Thestem, leaf, sheath and grains from 5 commonly plantedrice cultivars (Table 1) were used to determine thecontent of phytoliths and PhytOC in different organs,and to analyze the relationship of two aspects in dif-ferent rice cultivars and organs of the same rice plant.

The rice plant samples (three replicates) of differentcultivars were collected during the harvest season inOctober, 2010, from the regional trials of new varietiesof crops grown at the demonstration base of ZhejiangSoil and Fertilizer Station (30°56′06.3″N and 120°51′52.9″E) in Jiaxing, Zhejiang Province, southeast China.The Base is located in Hangjiahu Plain which experi-ences a typical subtropical humid monsoon climate,with an average annual precipitation of 1,200 mm. Theannual mean temperature is 16 °C and the number offrost free days is 230. Soil is classified as the Earth-cumuli-Orthic Anthrosols (CSSD 2012).

Phytoliths occluded C analysis

In the laboratory, the phytolith extraction of rice or-gans (around 50 mg each test) was undertaken withmicrowave digestion procedures (Parr et al. 2001).This process was followed by a Walkley–Black typedigest (Walkley and Black 1934) to thoroughly re-move extraneous organic materials in the samples

(Parr et al. 2010). Each phytolith extraction solutionwas used 0.8 mol/l potassium dichromate to examinethe extraneous organic materials outside of the phytolithcells. If the color of solution would not change within5 min, it showed that the extraneous organic materialsoutside of the phytoliths were thoroughly removed. Thephytoliths extracted were oven-dried at 75 °C for 24 h ina centrifuge tube of known weight. The samples wereallowed to cool and then weighed to obtain the phytolithquantities. Each sample was checked with an opticalmicroscope (Olympus CX31, Japan) to further ensurethat all extraneous organic materials outside of thephytoliths were thoroughly removed (Murphy 2002).Based on methods of Kroger et al. (2002), the driedphytoliths samples were treated with 1 mol/L HF at 45 °C for 60 min to dissolve phytolith-Si. The organic Creleased from phytoliths after HF treatment was dried at45 °C and determined for C content using the classicalpotassium dichromate method (Lu 2000). The organic Cdata was monitored with standard soil samples ofGBW07405. The precision is better than 7 %.

Results

Microscopy check show that all external organic mate-rials were completely removed (Fig. 1). The contents ofphytoliths in different rice organs (leaf, stem, sheath,grains) range from 15 mgg−1 to 144 mgg−1 and show asimilar trend (sheath>leaf>stem>grains) in 5 rice cul-tivars (Table 1). There are substantial variations in the Ccontent (14mgg−1–34mgg−1) of phytoliths from organsin rice cultivars (Table 1). Generally, the C content ofphytoliths from the stem is higher than that of sheath,grains and leaf (Table 1). The PhytOC contents oforgans on a dry weight basis in the 5 rice cultivars varyfrom 0.4 mgg−1 to 2.8 mgg−1 and have a consistenttrend (sheath>leaf>steam>grains) (Table 1).

A weak negative correlation exists between the con-tent of phytoliths and the C content of phytoliths fromdifferent organs in 5 rice cultivars (R2=0.2236, p>0.05)(Fig. 2). However, there are strong positive correlationsbetween the content of phytoliths and the PhytOCcontent of different organs (R2=0.8651, p<0.01)(Fig. 3). The correlation (R2=0.2733, p>0.05) betweenthe C content of phytoliths and the PhytOC content ofgrains is weaker than that of leaf (R2=0.8241, p<0.01),stem (R2=0.9214, p<0.01) and sheath (R2=0.5168,p<0.05) (Fig. 4).

Plant Soil

Discussion

The mechanism of C occlusion within rice phytolithsand its application

A number of researchers (e.g., Parr et al. 2009, 2010;Parr and Sullivan 2011; Zuo and Lü 2011) found thatthe PhytOC content in bamboo, wheat, sugarcane and

millet has no direct relationship with the actual contentof silica (phytoliths) taken up by the plant, and mainlydepends on the efficiency of the C occluded withinphytoliths during plant growth. However, our studyresults on C occlusion within rice phytoliths are quitedifferent from the above studies. The strong positivecorrelations between the phytolith content and thePhytOC content of organs in 5 rice caltivars tested

Table 1 Rice cultivars and organs, the phytolith content as apercentage of organs biomass, the PhytOC content of the ricephytoliths, the content of PhytOC in organs on a dry weightbasis and the estimated fluxes of PhytOC per ha in Mg of CO2

equivalents (Mg-e-CO2) for rice (according to grains yields ofsingle and double rice crops between 9.3 and 18.6 Mg-ha−1)

(data offered by Zhejiang Soil and Fertilizer Station)

Ricecultivars

Riceorgans

Phytolith contentsMean (s. d) mgg−1

PhytOC of phytolithsMean (s. d) mgg−1

PhytOC of organsMean (s. d) mgg−1

Estimated PhytOC fluxes(Mg-e-CO2 ha

−1year−1)

Xiushui 09 grains 20.56 (0.26) 20.16 (1.05) 0.41 (0.03) 0.04–0.10stem 30.87 (3.36) 21.06 (1.16) 0.65 (0.11)

sheath 132.95 (5.67) 21.27 (1.46) 2.83 (0.30)

leaf 55.47 (8.16) 18.66 (3.05) 1.04 (0.32)

Ning 81 grains 26.57 (3.86) 18.47 (1.57) 0.49 (0.13) 0.03–0.12stem 37.36 (11.56) 28.85 (8.36) 1.08 (0.65)

sheath 108.87 (3.76) 19.56 (1.14) 2.13 (0.20)

leaf 64.57 (9.18) 24.46 (1.36) 1.58 (0.32)

Xianghu 301 grains 27.23 (5.76) 23.47 (0.14) 0.63 (0.14) 0.05–0.13stem 39.12 (2.44) 33.56 (0.36) 1.31 (0.09)

sheath 118.57 (5.76) 20.47 (0.13) 2.43 (0.14)

leaf 77.87 (2.03) 22.13 (0.37) 1.72 (0.07)

Zhejing 37 grains 15.47 (1.48) 23.16 (0.27) 0.36 (0.04) 0.04–0.08stem 40.23 (2.27) 24.75 (0.46) 1.00 (0.08)

sheath 103.06 (2.37) 22.14 (1.14) 2.28 (0.16)

leaf 79.27 (5.24) 25.67 (1.47) 2.03 (0.25)

Jiahua 11 grains 21.57 (2.14) 26.16 (2.04) 0.56 (0.09) 0.04–0.11stem 39.95 (5.04) 27.27 (1.47) 1.09 (0.20)

sheath 143.95 (6.96) 14.18 (1.68) 2.04 (0.34)

leaf 74.57 (1.14) 23.01 (0.37) 1.72 (0.03)

Fig. 1 Rice phytolithsextracted by the microwavemethod followed by aWalkley–Black digest usingstandard light microscopy(Walkley and Black 1934;Parr et al. 2001)

Plant Soil

(R2=8651, P<0.01) (Fig. 3), and between the C con-tent of the phytoliths in each organ and the PhytOCcontent of organs in 5 rice caltivars (R2=0.2733–0.9214) (Fig. 4) indicate that the PhytOC content inrice plants might depend on both the content ofphytoliths and the nature of silica occluding C withincells of the phytoliths during plant growth. Thus, allfactors influencing the content of phytoliths and thecontent of silica occluding C within phytoliths couldresult in significant variations of the PhytOC contentin plants. For example, factors such as varieties, loca-tion, disease resistance, and fertilizer requirements canplay a major role in accumulating phytoliths duringplant growth (Ma et al. 2002; Korndorfer and Lepsch

2001; Ding et al. 2005; Parr and Sullivan 2011; Zuoand Lü 2011). The different shape of phytoliths be-tween different organs (e.g., between rice stem andrice sheath) may also cause differences in the C con-tent of phytoliths because of differences in specificsurface area (Table 1; Bartoli and Wilding 1980;Bartoli 1985). However, these indirect factors remainto be examined in further studies.

It is possible to improve the sequestration rate ofPhytOC simply by selecting cultivars of high-phytolith content and high-C content of phytolithsfor cropping (Parr et al. 2010; Parr and Sullivan2011). However, as pointed out by Parr et al. (2009)cultivars cannot be selected solely on the basis of theirPhytOC content but rather should be considered incombination with other desirable traits such as bio-mass and yield. In addition, other limiting factors,such as differences in location and climatic conditions(Parr et al. 2009; Parr and Sullivan 2011), and tastepreferences also need to be considered. As we haveshown in this study for rice there is a strong relation-ship between silica (phytolith) production and PhytOCcontent (Figs. 3 and 4) thus even if rice crops with arelatively weak ability for occluding C in theirphytoliths are planted, it may still be possible toenhence the PhytOC content for the plants by regulat-ing silicon supply during growing period. For exam-ple, previous studies have demonstrated that thecontent of the silica (phytoliths) in crops may beenhanced through adding manganese zinc silicon fer-tilizer, straw (Bao et al. 1996), organic fertilizer,calcium-magnesium phosphate fertilizer (Chen et al.

y = -0.051x + 26.09

R2 = 0.2241, P > 0.05

0

9

18

27

36

0 40 80 120 160

Phytolith content (mg g -1)

C c

onte

nt o

f ph

ytol

ith

(mg

g -1

)

Fig. 2 Correlation of the phytolith content of organs and the Ccontent of phytoliths in 5 rice cultivars

y = 0.0166x + 0.315

R2 = 0.8651, P < 0.01

0.0

1.0

2.0

3.0

0 40 80 120 160

Phytolith content (mg g-1)

Phyt

OC

con

tent

in o

rgan

s

(mg

g -1

)

Fig. 3 Correlation of the phytolith content of organs andPhytOC content of organs in 5 rice cultivars. (PhytOC contentin organs as a function of phytolith content)

y = 0.0494x + 1.304

R2 = 0.5168, P < 0.05

y = 0.1247x - 1.242

R2 = 0.8241, P< 0.01

y = 0.0174x + 0.1127

R2 = 0.2733, P > 0.05

y = 0.0474x - 0.2274

R2 = 0.9214, P < 0.01

0.0

1.0

2.0

3.0

0 5 10 15 20 25 30 35 40C content of phytoliths (mg g-1)

Phy

tOC

con

tent

in o

rgan

s

( m

g g

-1)

leafstemsheathgrains

Fig. 4 Correlation of PhytOC content of organs and the Ccontent of phytoliths in 5 rice cultivars. (PhytOC content inorgans as a function of the C content of phytoliths)

Plant Soil

2008), slag mucks (Zhang et al. 2008), and siliconfertilizers (Matichenkov et al. 1999; Alvarez andDatnoff 2001; Ma and Takahashi 2002; Liang et al.2006; Mecfel et al. 2007) during the plant growth. Infact, silica (phytolith) accumulation also provides plantswith some competitive advantages during the cropsgrowth, such as enhancement of yield and growth, re-sistance to disease and increased shoot rigidity, etc.(Epstein 2001) through the regulation of silicon nutrientsupply for crops. It is likely to enhance PhytOC contentin crops through regulating silicon nutrient supply forcrop plants in agricultural production.

Carbon sequestration potential through C occlusionwithin the phytoliths in rice plants

Using the PhytOC content of rice plant material on a dryweight basis (leaf, stem, sheath, grains) (Wang et al. 2008)and the mean annual production (9.3–18.6 Mg-ha−1) of

grains of the single and double rice cropping systems(Anthoni et al. 2004; Zhang et al. 2010), we estimate thatthe C flux of rice phytoliths is 0.03–0.13 Mg-e-CO2 ha

−1-year−1. Comparedwith the other studies (Table 2), the fluxof the phytolith C sequestration in this study is noticeablylower than that of bamboo, wheat and sugarcane (Parr etal. 2009; Parr et al. 2010; Parr and Sullivan 2011). Themain causes for this significant difference in PhytOCcontent may be as follows: a) the C content of phytolithsin the 5 rice cultivars tested is simply not as high as that forbamboo, wheat and sugarcane; b) the rice produces lessbiomass than other phytolith species, e.g., bamboo leaf(Parr et al. 2010), perhaps rice cultivars with strongerPhytOC traits are yet to be discovered or c) the methodof C quantification used in this study (Lu 2000) whichvaried considerably from previous studies (Parr et al.2009; Parr et al. 2010; Parr and Sullivan 2011) providesa significantly different result; d) Genetic reasons anddifferent physiology/relationship to water may affect the

Table 2 Comparison of PhytOC contents in plant tissues, estimated PhytOC fluxes per hat-CO2 equivalents and global total PhytOCsequestration rate in different plants

Plants species PhytOC contents of drymaterial (mgg−1)

PhytOC sequestration fluxes(Mg-e-CO2 ha

−1-year−1)Global PhytOC sequestrationrates (Mg -e-CO2 -year

−1)References

Rice 0.4–2.8 0.03–0.13 1.94×107 This study

Bamboo 2.4–5.2 0.01–0.71 1.56×107 Parr et al. 2010

Sugarcane 3.1–15.4 0.12–0.36 0.72×107 Parr et al. 2009

Wheat 0.6–6.0 0.01–0.25 5.3×107 Parr and Sullivan 2011

Millet 0.4–2.7 0.01–0.04 0.27×107 Zuo and Lü 2011

20

25

30

35

40

1950 1960 1970 1980 1990 2000 2010

Ric

e-pl

ante

d ar

ea (

10 6 h

a)

Fig. 5 The variation trend of rice planted-areas from 1950 to2010 in China (NBSC 2011 and CSDN 2011)

1.0

2.0

3.0

4.0

1950 1960 1970 1980 1990 2000 2010

C o

cclu

sion

rat

es (

10 6

Mg-

e-C

O2)

Fig. 6 Estimated the lowest and highest potential rate of CO2

sequestration through PhytOC accumulation in rice plants between1950 and 2010 in China

Plant Soil

C content of phytoliths in different plants. These are areas,which, while beyond the scope of the current study,necessarily require further investigation.

According to the records for the area of rice plantedfrom 1950 to 2010 in China (NBSC 2011 and CSDN2011) (Fig. 5), we have estimated the trend of the lowestand highest potential rates of CO2 occluded within ricephytoliths from 1950 to 2010 (Fig. 6). Our results estimatethat between 0.81×106 and 3.88×106Mg-e-CO2 per yearis occluded within the rice phytoliths in China. Applyingthe largest flux (0.13Mg-e-CO2 ha

−1year−1) of the largestPhytOC sequestration flux in this study, our results indi-cate that rice phytoliths have potentially occluded around2.37×108Mg-e- CO2 during the past 60 years. In 2010,the rice planting-area of the world was around 1.55×108

ha (IRRI 2011). Taking the largest flux (0.13 Mg-e-CO2

ha−1year−1) of rice phytoliths, about 1.94×107Mg-e-CO2

per year would have been sequestrated in rice phytolithsglobally. Although the annual CO2 occlusion within therice phytoliths of unit area is likely to be lower than that ofother plants such as bamboo, wheat and sugarcane(Table 2), based on the total area of rice production theglobal CO2 sequestration (1.94×10

7Mg-e-CO2 year−1) in

rice phytoliths is greater than those of reported, for exam-ple, bamboo leaf litter (1.56×107Mg-e-CO2 year

−1) (Parret al. 2010) and sugarcane leaf (0.72×106Mg-e-CO2

year−1) (Parr et al. 2009). When rice straw is returned tothe paddy fields, phytoliths are released into the soil afterstraw decomposition. The PhytOC from rice is very stableand can be preserved in soils for more than 6,000 years(Cao et al. 2006, 2007; Zheng et al. 2003). For example,fan type (bulliform cell) rice phytoliths could be foundintact in ancient paddy soil (6,280 a BP) at the Chuodunsite (Cao et al. 2007). Thus, the PhytOC can be consideredas an important part of soil stable organic C and plays animportant role in long-term C sequestration (Parr andSullivan 2005) and mitigation of global climate change(Parr et al. 2010; Parr and Sullivan 2011; Zuo and Lü2011). It is especially important to further quantify andenhance the potential of PhytOC of cultivated plants suchas rice and other arable crops under different soil andclimate conditions.

Conclusions

Our study reveals that the PhytOC content of the differ-ent organs (leaf, stem, sheath and grains) in 5 ricecultivars ranged from 0.4 mgg−1 to 2.8 mgg−1. The C

content of phytoliths in grains is much lower than that ofother organs, such as leaf, stem and sheath. The data alsoshow that the PhytOC content in rice mainly depends onboth the content of silica (phytoliths) and the efficiencyof the C occluded within phytoliths during rice growth.Based on our results, it is estimated that the flux of Coccluded within rice phytoliths is between 0.03 and0.13 t-e-ha−1-year−1. Rice may sequester between0.81×106 and 3.88×106Mg-e-CO2 annually and up to2.37×108Mg-e-CO2 within phytoliths of cultivated riceduring a 60-year period in China. According to theglobal rice planting area (1.55×108ha), we estimate that1.94×107Mg-e-CO2 from the atmosphere could havebeen sequestered in rice phytoliths annually, whichcould play an important role in mitigation of globalgreenhouse gas emission. However, more studies onthe capacity of the PhytOC accumulation in arable cropsare needed to quantify potential of phytoliths in global Csequestration and to reduce greenhouse gas concentra-tion in the atmosphere.

Acknowledgments We are grateful for support from NationalNatural Science Foundation of China (Grant No. 41103042), Zhe-jiang Province Key Science and Technology Innovation Team(NO.2010R50030), Zhejiang Provincial Natural Science Founda-tion Program (Grant No. Y5080110 and Z5080203), Opening Pro-ject of State Key Laboratory of Environmental Geochemistry(SKLEG9011), Opening Project of Ministry of Education Labora-tory for Earth Surface Processes, Peking University. We thank Pr.Dr. Zhihong Cao and Miss Fang Huang for their help in sampling.

References

Alvarez J, Datnoff LE (2001) The economic potential of siliconfor integrated management and sustainable rice production.Crop Prot 20:43–48

Anthoni PM, Freibauer A, Kolle O, Schulze E (2004) Winterwheat carbon exchange in Thuringia, Germany. Agr ForMeteorol 121:55–67

Baker G (1961) Opal phytoliths and adventitious mineral parti-cles in Wheat dust. CSIRO, Melbourne

Baker G, Jones LHP, Wardro ID (1961) Opal phytoliths andmineral particles in the rumen of sheep. Aust J Agric Res12:462–471

Bao SD, Yang XR, Li XQ, Zhang MJ (1996) The effect of wheatyields on silicon nutrition and the zinc silicon fertilizer incalcareous soils. Soil 6:311–315 (In Chinese)

Bartoli F (1985) Crystallochemistry and surface properties ofbiogenic opal. J Soil Sci 36:335–350

Bartoli F, Wilding LP (1980) Dissolution of biogenic opal as afunction of its physical and chemical properties. Soil SciSoc Am J 44:873–878

Plant Soil

Bowdery D (2007) Phytolith analysis: sheep, diet and fecalmaterial at Ambathala Pastoral Station, Queensland, Aus-tralia. In: Madella M, Débora Z (eds) Plant, people andplaces–recent studies in phytolith analysis. Oxbow, Oxford

Cao ZH, Zhang HC (2004) Phosphorus losses to water fromlowland rice fields under rice-wheat double cropping sys-tem in the Tai Lake region. Environ Geochem Health26:229–236

Cao ZH, Ding JL, Hu ZY, Knicker H, Kögel-Knabner I, YangLZ, Yin R, Lin XG, Dong YH (2006) Ancient paddy soilsfrom the Neolithic age in China’s Yangtze River Delta.Naturwissenschaften 93:232–236

Cao ZH, Yang LZ, Lin XG, Hu ZY, Dong YH, Zhang GY et al(2007) Morphological characteristics of paddy fields, pad-dy soil profile, phytoliths and fossil rice grain of the Neo-lithic age in Yangtze River Delta. Acta Pedologica Sin44:839–847 (In Chinese)

Chen JG, Zhang YZ, Zeng XB, Zhou WJ, Zhou J (2008) Effectof long-term various fertilization on exchangeable Ca andMg, and available S and Si contents in paddy soils. EcolEnviron 17:2064–2067

China Sannong Data NetWork (CSDN) (2011) http://www.sannong.gov.cn

China Soil Scientific Database (CSSD) (2012) http://mirror.soil.csdb.cn/page/showItem. vpage?id=cn. csdb. soil. tax-onomy. cst Yagang/

Clark DA (2002) Are tropical forests an important carbon sink?Reanalysis of the long-term plot data. Ecol Appl 12:3–7

Ding TP, Ma GR, Shui MX, Wan DF, Li RH (2005) Siliconisotope study on rice plants from Zhejiang Province, Chi-na. Chem Geol 218:41–50

DOE (2008) International Energy Outlook 2008 Energy Infor-mation Administration Office of Integrated Analysis andForecasting. US. Department of Energy, Washington, DC

Epstein E (1994) The anomaly of silicon in plant biology. ProcNatl Acad Sci USA 91:11–17

Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant MolecBiol 50:641–644

Epstein E (2001) Silicon in plants: facts vs. concepts. In:Datnoff LE, Snyder GH, Korndorger GH (eds) Silicon inagriculture). Elsevier Science B.V, Amsterdam, pp 1–15

Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J,Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT,Moore B III, Pedersen T, Rosenthal Y, Seitzinger S, SmetacekV, Steffen W (2000) The global carbon cycle: a test of ourknowledge of earth as a system. Science 290:291–296

Fang JY, Guo ZD, Piao SL, Chen AP (2007) Terrestrial vegeta-tion carbon sinks in China, 1981–2000. Sci China Ser D-Earth Sci 50:1341–1350

Field CB (2001) Plant physiology of the “Missing” carbon sink.Plant Physiol 125:25–28

Gifford RM (1994) The global carbon cycle: a viewpoint on themissing sink. Aust J Plant Biol 21:1–15

Harrison K, Broecker W, Bonani G (1993) A strategy for esti-mating the impact of CO2 fertilization on soil carbonstorage. Global Biogeochem Cy 7:69–80

Hart DM, Humphreys GS (1997) Plant opal phytoliths: anAustralian perspective. Quatern Aust 15:17–25

Intergovernmental Panel on Climate Change (IPCC) (2007)Climate change 2007: the scientific basis. Cambridge Uni-versity Press, UK

International Rice Research Institute (IRRI) (2011) http://beta.irri.org/

Jones L, Handreck K (1967) Silica in soils, plants and animals.Adv Agron 19:107–149

Jones LHP, Milne AA (1963) Studies of silica in the oat plant.Plant Soil XVIII:207–220

Korndorfer GH, Lepsch I (2001) Effect of silicon on plant growthand crop yield. In: Datnoff LE, Snyder GH, Korndorfer GH(eds) Silicon in agriculture. Elsevier Science BV, Amsterdam

Kosten S, Roland F, Da Motta Marques DML, Van Nes EH,Mazzeo N, Stemberg LDSL, Scheffer M, Cole JJ (2010)Climate-dependent CO2 emissions from lakes. GlobalBiogeochem Cy 24. doi:10.1029/2009GB003618

Kroger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their func-tion in biosilica morphogenesis. Science 298:584–586

Liang Y, Hua H, Zhu YG, Cheng C, Romheld V (2006) Impor-tance of plant species and external silicon concentration toactive silicon uptake and transport. New Phytol 172:63–72

Lin XG, Yin R, Zhang HY, Huang JF, Chen RR, Cao ZH (2004)Changes of soil microbiological properties caused by landuse changing from rice-wheat rotation to vegetable culti-vation. Environ Geochem Health 26:119–128

Lu RK (2000) Methods for soil and agrochemical analysis.China Agriculture Press, Beijing

Ma JF, Takahashi E (2002) Amsterdam: Elsevier Science; Soil,fertilizer, and plant silicon research in Japan, 1st edn.Elsevier Science, Amsterdam

Ma JF, Tamai K, Ichii M, Wu K (2002) A rice mutant defectivein active Si uptake. Plant Physiol 130:2111–2117

Matichenkov V, Calvert D, Snyder G (1999) Silicon fertilizersfor citrus in Florida. Proc Fla State Hort Soc 112:5–8

McKenzie N, Ryan P, Fogarty P, Wood J (2000) Sampling,measurement and analytical protocols for carbon estima-tion in soil, litter and coarse woody debris, AustralianGreenhouse Office, National Carbon Accounting System,Technical Report no 14:1–42

Mecfel J, Hinke S, Goedel WA, Marx G, Fehlhaber R, BǎuckerE, Wienhaus O (2007) Effect of silicon fertilizers onsilicon accumulation in wheat. J Plant Nutr Soil Sci170:769–772

Mulholland SC, Prior CA (1993) AMS radiocarbon dating ofphytoliths. In: Pearsall DM, Piperno DR (eds) MASCAresearch papers in science and archaeology. University ofPennsylvania, Philadelphia, pp 21–23

Murphy D (2002) Fundamentals of light microscopy and elec-tronic imaging. A John Wiley & Sons, Inc., 121 pp

National Bureau of Statistics of China (NBSC) (2011) http://www.stats.gov.cn/

Oldenburg CM, Torn MS, DeAngelis KM, Ajo-Franklin JB,Amundson RG, Bernacchi CJ, et al. (2008) Biologicallyenhanced carbon sequestration: Research needs opportuni-ties. Report on the Energy Biosciences Institute Workshopon Biologically Enhanced Carbon Sequestration, October29 2007, Berkeley, CA, LBNL–713E

Parr JF (2006) Effect of fire on phytolith coloration. Geo-archaeology 21:171–185

Parr JF, Sullivan LA (2005) Soil carbon sequestration inphytoliths. Soil Biol Biochem 37:117–124

Parr JF, Sullivan LA (2011) Phytolith occluded carbon and silicavariability in wheat cultivars. Plant Soil 342:165–171

Plant Soil

Parr JF, Dolic V, Lancaster G, Boyd WE (2001) A microwavedigestion method for the extraction of phytoliths fromherbarium specimens. Rev Palaeobot Palynol 116:203–212

Parr JF, Sullivan LA, Quirk R (2009) Sugarcane phytoliths:encapsulation and sequestration of a long-lived carbonfraction. Sugar Tech 11:17–21

Parr JF, Sullivan LA, Chen B, Ye G, Zheng W (2010) Carbonbio-sequestration within the phytoliths of economic bam-boo species. Global Change Biol 16:2661–2667

Pearsall DM (1989) Paleoethnobotany: a handbook of proce-dures. Academic, London

Perry CC, Williams RJP, Fry SC (1987) Cell wall biosynthesisduring silicification of grass hairs. J Plant Physiol 126:437–448

Piperno DR (1988) Phytolith analysis: an archaeological andgeological perspective. Academic, London

Prasad V, Strömberg CAE, Alimohammadian H, Sahni A (2005)Dinosaur coprolites and the early evolution of grasses andgrazers. Science 310:1177–1180

Sangster AG, Parry DW (1981) Ultrastructure of silica depositsin higher plants. In: Simpson TL, Volcani BE (eds) Siliconand siliceous structures in biological systems. Springer,New York, pp 383–407

Schimel D (1995) Terrestrial ecosystems and the carbon cycle.Global Change Biol 1:77–91

Schlesinger WH (1997) Biogeochemistry: an analysis of globalchange. Academic, New York

Skjemstad JO, Spouncer LR, Beech A (2000) Carbon conver-sion factors for historical soil carbon data. 15, CSIRO Landand Water, Adelaide

Song ZL, Liu HY, Si Y, Yin Y (2012a) The production ofphytoliths in China’s grasslands: implications to the bio-geochemical sequestration of atmospheric CO2. GlobalChange Biol 18:3647–3653

Song ZL, Wang HL, Strong PJ, Li ZM, Jiang PK (2012b) Plantimpact on the coupled terrestrial biogeochemical cycles of

silicon and carbon: Implications for biogeochemical carbonsequestration. Earth Sci Rev 319–331

Strömberg CAE (2004) Use phytolith assemblages to reconstructthe origin and spread of grass-dominated habitats in the greatplains of North America during the late Eocene to earlyMiocene. Paleogeogr Paleoclimatol Paleoecol 207:239–275

Walkley A, Black IA (1934) An examination of the Degtjareffmethod for determining soil organic matter, and a proposedmodification of the chromic acid titration method. Soil Sci37:29–38

Wang SM, Zhang CH, Hu FX, Zeng K, Zhang WH, Wang WJ(2008) The quantitative analysis of rice aboveground bio-mass and net primary productivity. Chinese Agr Sci Bull24:201–205 (In Chinese with English abstract)

Wilding LP (1967) Radiocarbon dating of biogenetic opal.Science 156:66–67

Wilding LP, Drees LR (1974) Contributions of forest opal andassociated crystalline phases to fine silt and clay fractionsof soils. Clay Clay Miner 22:295–306

Wilding LP, Brown RE, Holowaychuk N (1967) Accessibilityand properties of occluded carbon in biogenetic opal. SoilSci 103:56–61

Zhang YL, Yu L, Liu MD, Yu N (2008) Silicon liberationcharacteristics of soil and its effect factors after applyingslag mucks I Relationships between Calcium, Magnesium,Iron and Aluminium and Silicon liberation. Chinese J SoilSci 39:722–725 (In Chinese)

Zhang WJ, Wang XJ, Xu MG, Huang SM, Peng C (2010) Soilorganic carbon dynamics under long-term fertilizations inarable land of northern China. Biogeosciences 7:409–425

Zheng Y, Matsui A, Fujiwara H (2003) Phytoliths of ricedetected in the Neolithic sites in the valley of the TaihuLake in China. Env Archaeol 8:177–184

Zuo XX, Lü HY (2011) Carbon sequestration within milletphytoliths from dry-farming of crops in China. ChineseSci Bull 56:3451–3456

Plant Soil