Silicon’s organic pool and biological cycle in moso bamboo community of Wuyishan Biosphere Reserve

Silicon’s organic pool and biological cycle in moso bamboo community of Wuyishan Biosphere Reserve 1 first-author †E-mail:zhenjil@163.com †E-mail:zhenjil@163.com zhenjil@163.com 1 2 1 1 College of Life Sciences, Xiamen University, Xiamen 361005, China College of Life Sciences, Xiamen University, Xiamen 361005, China Administrative Bureau of Wuyishan National Nature Reserve, Wuyishan 354315, China Administrative Bureau of Wuyishan National Nature Reserve, Wuyishan 354315, China Biomineralization of Si by plants into phytolith formation and precipitation of Si into clays during weathering are two important processes of silicon’s biogeochemical cycle. As a silicon-accumulating plant, the widely distributed and woody Phyllostachys heterocycla var. pubescens (moso bamboo) contributes to storing silicon by biomineralization and, thus, prevents eutrophication of nearby waterbodies through silicon’s erosion of soil particles. A study on the organic pool and biological cycle of silicon (Si) of the moso bamboo community was conducted in Wuyishan Biosphere Reserve, China. The results showed that: (1) the standing crop of the moso bamboo community was 13355.4 g/m 2 , of which 53.61%, 45.82% and 0.56% are represented by the aboveground and belowground parts of moso bamboos, and the understory plants, respectively; (2) the annual net primary production of the community was 2887.1 g/(m 2 ·a), among which the aboveground part, belowground part, litterfalls, and other fractions, accounted for 55.86%, 35.30%, 4.50% and 4.34%, respectively; (3) silicon concentration in stem, branch, leaf, base of stem, root, whip of bamboos, and other plants was 0.15%, 0.79%, 3.10%, 4.40%, 7.32%, 1.52% and 1.01%, respectively; (4) the total Si accumulated in the standing crop of moso bamboo community was 448.91 g/m 2 , with 99.83% of Si of the total community stored in moso bamboo populations; (5) within moso bamboo community, the annual uptake, retention, and return of Si were 95.75, 68.43, 27.32 g/(m 2 ·a), respectively; (6) the turnover time of Si, which is the time an average atom of Si remains in the soil before it is recycled into the trees or shrubs, was 16.4 years; (7) the enrichment ratio of Si in the moso bamboo community, which is the ratio of the mean concentration of nutrients in the net primary production to the mean concentration of nutrients in the biomass of a community, was 0.64; and lastly, (8) moso bamboo plants stored about 1.26×10 10 kg of silicon in the organic pool made up by the moso bamboo forests in the subtropical area of China. Phyllostachys heterocycla var. pubescens Moso bamboo community Silicon-accumulating Silicon biological cycle Wuyishan Biosphere Reserve INTRODUCTION 1 Silicon (Si), the element in many plant biologists’ minds, as we come into an age of research ‘ in silico ’, still is an enigma when it comes to its nutritional role in the higher land plants (Raven, 2003 2003 ). The element occurs in the soil solution at 0.1~0.6 mol/m 3 as Si(OH) 4 (two orders of magnitude higher than the macronutrient phosphorus (H 2 PO 4 − /HPO 4 2− )) (Epstein, 1999 1999 ). Although silicon is not an essential element for higher plants, it is an important nutrient for phytoplankton and is easily absorbed by terrestrial plants, especially gramineous plants (Li and Lin, 1995 1995 ; Liu, 1996 1996 ; Alexandre et al., 1997 1997 ; Raven, 2003 2003 ; Basile-Doelsch et al., 2005 2005 ). Silicon can improve efficiency of water use and decrease both biotic and abiotic stresses in plants (Epstein, 1994 1994 ; Liang, 1999 1999 ; Gao et al., 2004 2004 ), and can also enhance plant tolerance of drought; this is attributed to increased selectivity in ion uptake by plant cells (Liang, 1999 1999 ). Also Si can help plants recover from wound (Pereira and Felcman, 1998 1998 ) and can also assist in the fixation and removal of carbon dioxide from the atmosphere through its weathering (Berner, 1997 1997 ; Liese, 2001 2001 ; Graetz and Skjemstad, 2003 2003 ; Derry et al., 2005 2005 ). But the continental cycle of silicon is not well known and the attempts to associate Si with metabolic or physiological activities have been inconclusive (Epstein, 1994 1994 ; Liang, 1999 1999 ; Basile-Doelsch et al., 2005 2005 ). Basile-Doelsch et al.( 2005 2005 ) suggested that the re-precipitation of quartz plays an important role in the biogeochemical cycle of silicon. Traditionally, two processes that fractionate Si isotopes have been suspected: biomineralization of Si by plants into phytolith formation and precipitation of Si into clays during weathering (Basile-Doelsch et al., 2005 2005 ). Among different plants, the gramineous plants have been classified as silicon-accumulators (Takahashi and Miyake, 1976 1976 ; Li and Lin, 1995 1995 ; de Bakker et al., 1999 1999 ). Phyllostachys heterocycla (Carr.) Matsum. var. pubescens (Mazet) Owhi (moso bamboo), a typical silicon-accumulating plant, is widely distributed in China. Moso bamboo community is an important forest type dominated by woody and silicon-rich bamboos (Poaceae) and is distributed widely from Taiwan in the east to Sichuan in the west, from Guangdong in the south to Henan in the north, and from plain to mountain (Wu, 1980 1980 ; Chen, 1984 1984 ). We proposed that the moso bamboo community is an important organic silicon pool in terrestrial ecosystem. Here we focus on it with case study conducted at one of the central areas of its overall distribution range—Wuyishan Biosphere Reserve. SITE DESCRIPTION 1 Wuyishan Biosphere Reserve locates in the northern part of the subtropical province of Fujian in China, covers a total area of 56527 hm 2 (Fig. 1 1 ). The reserve has been well known for its ecosystem diversity and also its species and genetic richness for plants, insects, birds and reptiles (Li et al., 2004 2004 ). It became a national nature reserve in China in 1979, and was accepted as a MAB Reserve by UNESCO in 1987. Because of its lofty peaks and deep gorges, this area provided habitats for many vegetation types and is characterized by abundant biodiversity (Lin and Ye, 1993 1993 ). The study site (27°42′ N, 117°41′ E), Dazhulan in Wuyishan Biosphere Reserve, has mountainous topography, southeast-facing slope of 20°, and altitude of 1100 m (Fig. 1 1 ). Evergreen broadleaved and moso bamboo forests dominated the natural areas at low altitudes in this subtropical region (Wu, 1980 1980 ; Lin, 1986 1986 ). The moso bamboo ( Phyllostachys heterocycla var. pubescens ) community is a natural vegetation dominated by mature moso bamboo plants (i.e., 14~20 cm dbh (diameter breast high), 17.5 m in mean height) with density of 1900 individuals/hm 2 . The understory is fairly open, consisting of Eurya nitida , Lindera aggregata , Liriope platyphylla , Dryopteris fuscipes , Alpinia japonica , Lonicera japonica , Millettia dielsiana , and the seedlings of Castanopsis eyrei , Cunninghamia lanceolata , and Cyclobalanopsis glauca . The underlying bedrock is volcanic lava. Soil is characterized as mountain yellow earth, 50~110 cm in depth, and covered with a litter layer of 5 cm consisting of 4.52%~6.43% of soil organic matters with pH of 4.5~5.5. The climate at the study site is monsoonal and subtropical maritime, with mean annual temperature of 12.8 °C; the monthly averages ranging from 5.6 °C in January to 21.7 °C in July. The annual relative humidity and rainfall are 86.6% and 2678.8 mm. The highest precipitation occurs in June (average of 1143 mm). Solar duration is 1434.3 h and the annual mean wind speed is 0.91 m/s (Li et al., 2000 2000 ). MATERIALS AND METHODS 1 Sampling methods 2 1. Aboveground bamboo biomass 3 Aboveground bamboo biomass was calculated using forest inventory and regression techniques (Li et al., 1993 1993 ). We established four 10 m×10 m plots at each site and measured the diameter breast high (dbh) of all bamboos and other woody trees that were greater than 2.5 cm in diameter. A total of 8 bamboo trees, i.e., two pieces each of one year growth, three years growth and five years growth with 12 cm (dbh), and one piece of bamboo tree with 10 cm and 14 cm each, were harvested for biomass measurement and for Si measurement in stems, branches, leaves, base of stem, root and whip. These measurements were converted to biomass using bamboo-specific equations derived from our studies in southern Fujian (Li et al., 1993 1993 ). Understory plants and litter were sampled in another four plots measuring 5 m×5 m. Subsamples were collected from homogenized component samples to determine the total dry mass at 70 °C. 2. Root biomass 3 Root and whip biomass were collected at every 10 cm interval of soil layer within a total depth of 110 cm in four random plots measuring 1 m×1 m in each sampling plot (Li et al., 1993 1993 ). Soil and root weights were measured as the subsamples were collected. Root materials were separated and washed. All roots and whips samples measuring < 2 mm, 2~5 mm, > 5 mm diameter were collected and separated into live and dead fractions based on visual identification. 3. Net primary productivity (NPP) 3 We calculated NPP by the increases in biomass plus the litter production, sheaths, production of understory plants and dead shoots (Li et al., 1993 1993 ). The increment of living bamboo plant biomass was converted to NPP using bamboo-specific equations derived from our studies in south Fujian (Li et al., 1993 1993 ). Litterfall was collected at 10 d intervals in 20 traps that measured 1 m×1 m in size, randomly placed on the forest floor. The biomass increment for bamboo and the understory plants was calculated with species-specific equations (Li et al., 1993 1993 ). The weight of masses of living and dead roots was taken from the core samples of soil removed from the four plots at every 10 cm interval. Measurements of dead shoots were obtained in April from four random 5 m×5 m plots. These samples were oven dried at 70 °C to obtain a consistent dry weight. Biomass of the understory plants was estimated by harvesting seasonally also from another 4 random plots measuring 5 m×5 m. 4. Si content measurement 3 Each sample obtained for Si measurement was made up of about 250 g of composite plant materials consisting of the harvested uniform bamboos, litterfall, dead shoots and understory plants. All samples were dried at 70 °C and weighed to determine the mass per area (MA). Si content was measured by gravimetric method (Nayar et al., 1977 1977 ). Calculation 2 The calculation of turnover time, which is the average time the nutrient remains in the soil before it is recycled into the trees or shrubs, was achieved by the rate of the nutrients accumulating in the standing crop of a community and the mass of nutrients by annual return (Woodwell et al., 1975 1975 ). The enrichment ratio of nutrients refers to the ratio of the mean concentration of nutrients in the net primary production to the mean concentration of nutrients in the biomass of a community (Woodwell et al., 1975 1975 ). RESULTS 1 Biomass and productivity in moso bamboo community 2 1. Biomass and standing crop of moso bamboo community 3 The standing crop of the moso bamboo community was 13355.4 g/m 2 , of which, the aboveground part of the moso bamboo biomass was 7160 g/m 2 , representing 53.61%; the underground part of moso bamboo was 6120 g/m 2 , representing 45.82%; and understory plants was 75.4 g/m 2 , representing only 0.56% (Fig. 2 2 ). 2. Productivity of moso bamboo community 3 The annual net primary production of the moso bamboo community was calculated to be 2887.1 g/(m 2 ·a), in which, the aboveground part of moso bamboo plants contributed 55.86%, the belowground part, 35.30%, litterfalls, 4.50%, and other fractions, 4.34% (Table 1 1 ). Fraction Annual net primary production (g/(m 2 ·a)) Percentage to total (%) Aboveground part of moso bamboo 1612.81 55.86 Underground part of moso bamboo 1079.25 35.30 Understory plants 75.40 2.61 Litterfalls of moso bamboo 129.89 4.50 Dead bamboo shoots 20.15 0.70 Sheaths of bamboo shoots 29.60 1.03 Total annual net primary production 2887.10 100.00 Silicon content and storage in moso bamboo community 2 1. Silicon content in the biomass 3 The silicon concentration in stem, branch, leaf, base of stem, root, and whip of bamboos and other plants were calculated to be 0.15%, 0.79%, 3.10%, 4.40%, 7.32%, 1.52% and 1.01% respectively (Fig. 3 3 ). S: Stem; Br: Branch; L: Leaf; Bs: Base of stem; R: Root; W: Whip; U: Understory plants 2. Silicon storage in moso bamboo community 3 Silicon mainly stored in roots compared to other organs of bamboos (Fig. 4 4 ). The amount of Si stored in bamboos accounted for 99.83% of the total silicon accumulated to 448.91 g/m 2 in the moso bamboo community. In the bamboo plants, 79.41% is stored in root, and 11.08% in stem. Retention, return and uptake of silicon in moso bamboo community 2 In the moso bamboo community, silicon retention was 68.43 g/(m 2 ·a) (Table 2 2 ), return was 27.32 g/(m 2 ·a) (Table 3 3 ) and uptake was 95.75 g/(m 2 ·a). Item Stem Branch Leaf Base of stem Whip Root Understory plants Total Production (g/(m 2 ·a)) 1794.34 250.18 355.29 410.29 344.14 575.72 75.40 3805.36 Concentration of Si (%) 0.15 0.79 3.10 4.40 7.32 1.52 1.01 – Si-accumulating (g/(m 2 ·a)) 2.69 1.98 11.01 18.05 25.19 8.75 0.76 68.43 Item Leaf Branch Understory plants Dead shoots Bamboo sheaths Dead root Cut bamboo Total Production (g/(m 2 ·a)) 111.97 7.01 10.91 20.15 29.60 181.23 2124.90 2485.77 Concentration of Si (%) 7.36 0.79 1.01 1.09 9.37 4.52 0.36 – Si-accumulating (g/(m 2 ·a)) 8.25 0.06 0.11 0.22 2.77 8.19 7.72 27.32 As indicated in Tables 2 2 and 3 3 , 27.32 g/(m 2 ·a) (33.37% of silicon absorbed by moso bamboo community) are returned to the soil. Turnover time and enrichment ratio of Si in moso bamboo community 2 For the Si element in moso bamboo community of Wuyishan Biosphere Reserve, the turnover time was 16.4 years, and the enrichment ratio was 0.640. This means that Si does not accumulate long in the moso bamboo community. DISCUSSION 1 Biomass and productivity of moso bamboo community 2 Comparing the biomass and NPP of moso bamboo communities obtained from different areas in China (Table 4 4 ), we can notice that the biomass changes significantly in different places due to the management and temperature factors. The higher standing crop calculation at Yixing, Jiangsu (Zhou, 1987 1987 ), Fenghua, Zhejiang (Wen, 1990 1990 ) and Chishui, Guizhou (Wu, 1983 1983 ) is due to better management. At the center of the distribution range of moso bamboo communities, the amount of biomass changed from 12012 to 18240 g/m 2 due to good management practices (Huang et al., 1993 1993 ). In the periphery of its distribution, the calculated standing crop was as low as 6475~8289 g/m 2 (Peng et al., 2002 2002 ; Li et al., 1993 1993 ) due to the temperature, or other factors. Not including the data from Taiwan Site Location Biomass (g/m 2 ) NPP (g/(m 2 ·a)) Cited Yixing, Jiangsu 31°19′ N, 119°38′ E 27051 – Zhou, 1987 1987 Fuyang, Zhejiang 30°4′ N, 119°55′ E 18240 2252 Huang et al., 1993 1993 Fenghua, Zhejiang 29°37′ N, 121°20′ E 21609 2701.5 Wen, 1990 1990 Chishui, Guizhou 28°33′ N, 105°43′ E 26538 – Wu, 1983 1983 Wuyishan, Fujian 27°42′ N, 117°41′ E 13355.4 2887.1 This paper Yongchun, Fujian 25°27′ N, 117°40′ E 6475 – Peng et al., 2002 2002 Hubeliao, Fujian 24°56′ N, 117°14′ E 8289 2146.7 Li et al., 1993 1993 Chiton, Taiwan 23°39′ N, 120°48′ E 5545 (aboveground) 1110 (aboveground) Wang, 1981 1981 Mean * * – 17365 2499 – Moso bamboo is a widely distributed plant in China. Other works on this plant community conducted in Guangxi, Hubei and other areas focus on its structure or nutrition diagnosis (Nie, 1992 1992 ; Chen et al., 2004 2004 ). The productivity of the moso bamboo community varied from 2146 to 2887 g/(m 2 ·a) in northern area. We think that this is affected mainly by temperature. The annual productivity of moso bamboo community of Wuyishan Biosphere Reserve was higher than some bamboo communities occurring elsewhere, but due to the relatively poor management, the biomass measurement is still lower than that reported from areas such as Yixing in Jiangsu Province, and Fenghua in Zhejiang Province. This means that in northern Fujian, there is a potential to improve on the management and enhance its biomass production. In comparison, the moso bamboo community productivity is still higher than that reported for the evergreen broadleaved community (about 1382~1922 g/(m 2 ·a)) in the same subtropical zone (Dang and Wu, 1994 1994 ; Lin et al., 1996 1996 ; Sun, 2005 2005 ). This means that the moso bamboo community is a good sustainable forest to have in the China countryside. Concentration and storage of Si in moso bamboo community 2 The results of our study showed that the silicon concentration in organs of moso bamboo plants ranges from 0.15% to 7.32%. In a similar study on moso bamboo community in Asia, the silicon concentration ranges from 0.10% to 7.6% in various organs of moso bamboo plants (Takahashi et al., 1981 1981 ; Huang, 1983 1983 ; Chen, 1984 1984 ; Lux et al., 2003 2003 ). In the organs of other bamboo plants, Pleioblastus amarus and Phyllostachys praecox f. preveynalis , it ranges from 1.10% to 6.43% (Jiang and Yu, 2000 2000 ; Liu et al., 2004 2004 ). In the stem of Spartina anglica , the silicon concentration ranges between 0.35% and 1.17% (de Bakker et al., 1999 1999 ). Most researchers agree that the content of silicon is higher in gramineous plants than in non-gramineous plants. Our study showed further that the amount of silicon stored in the moso bamboo community of the Wuyishan Biosphere Reserve reaches to 448.15 g/m 2 . This may explain why the growth of moso bamboo community is better here in the central area of the range of this type of community when compared to the same bamboo community growing at the southern periphery of the range where the silicon contents of the bamboo community is a low 70.03 g/m 2 (Li and Lin, 1995 1995 ). Usually, silicon concentration in non-gramineous plants is lower than 2% (Lu and Wu, 1991 1991 ; de Bakker et al., 1999 1999 ). Silicon is an important nutrient for gramineous pasture plants, gramineous crops and bamboo plants. Abundant supply of SiO 2 can increase therefore the production of these plants substantially, and increase also their resistance to injury by diseases (Winslow et al., 1997 1997 ; Li et al., 1998a 1998a ; Xu et al., 2004 2004 ). This research showed that Si is important in moso bamboo community. Its concentration and deposition in the bamboos is much higher than those of other nutrient elements. The Ca storage in some tropical forests are reported to be as high as 6.8~11.3 g/m 2 in the aboveground part (Jiang and Lu, 1991 1991 ), and in some subtropical evergreen broadleaved forests, it is reported to be as high as 103.0~201.9 g/m 2 (Li et al., 1998b 1998b ; Liu et al., 1995 1995 ), but in moso bamboo community the amount of Ca storage is as low as 5.84~9.83 g/m 2 . According to the findings above, we propose, in addition, that in gramineous pasture plants, gramineous crops and bamboo plants, Si may serve as substitute for Ca in some ways. Biogeochemical cycle of Si in moso bamboo community 2 Biogeochemical cycle refers to natural processes that recycle nutrients in various chemical forms from the nonliving environment to living organisms, and then back to the nonliving environment (Miller, 2001 2001 ). The uptake of silicon in moso bamboo community was shown in this study to be 95.75 g/(m 2 ·a). The figures are much higher than those reported for N (9.46 g/(m 2 ·a)), P (0.43 g/(m 2 ·a)) (Lin et al., 1997 1997 ), Na (0.178 g/(m 2 ·a)) (Lin et al., 1998 1998 ), Mg (1.87 g/(m 2 ·a)) (Li et al., 1998b 1998b ), Ca (4.66~19.94 g/(m 2 ·a)), K (1.80~14.49 g/(m 2 ·a)) (Sun, 2005 2005 ) in broadleaved forests in the same subtropical zone. In the case of silicon, 74.98% of which is shown to be retained in the bamboo plants, while the remaining portion in its organic form is returned to the soil. This means that moso bamboo community can efficiently take up and accumulate silicon from arid soil and use it to support its growth in height; thus, the moso bamboo community contributes to prevent silicon erosion greatly. Our study also showed that silicon was not recycled and accumulated further in the moso bamboo community of Wuyishan Biosphere Reserve, probably because the community is located inside the nature reserve and is being protected; so the old individual bamboo trees are not harvested. In other moso bamboo communities elsewhere, it is advisable to continue to remove the old bamboo trees in order to help recycle this element by absorbing it from the soil. Estimation of Si accumulation in organic pool by moso bamboo community in China 2 Si accumulated in leaves and roots represents a huge biological pool of Si in area covered with bamboo vegetation. It has been demonstrated that a mat of fine roots developed by the bamboo community serves as an efficient nutrient recovery mechanism by minimizing the loss brought about by leaching to the subsoil in tropical forests (Stark and Jordan, 1978 1978 ). Moreover, deeply penetrated bamboo roots (up to a depth of 75 cm) are thought to constitute a ‘nutrient pump’ that recovers nutrients from the lower part of the soil horizon (Christanty et al., 1997 1997 ; Hu et al., 1994 1994 ). According to this research, at the center of the range of moso bamboo forests, 3754.8 kg of biogenic Si is present in soil per hm 2 . Take the whole distribution of bamboo forests in China, the moso bamboo forests, with coverage area of over 2.8×10 6 hm 2 throughout the subtropical region (Huang and Zhang, 1992 1992 ), can store about 1.26×10 10 kg silicon in the organic pool. This shows that the moso bamboo plants contribute greatly to the storing of silicon by the biomineralization process. This may prevent eutrophication of nearby waterbodies through the growth of diatoms brought by soil erosion. References A Alexandre , JD Meunier , F Colin , JM Koud . Plant impact on the biogeochemical cycle of silicon and related weathering processes . Geochim Cosmochim Acta , 1997 . 61 ( 3 ): 677 - 682 . DOI: 10.1016/S0016-7037(97)00001-X http://doi.org/10.1016/S0016-7037(97)00001-X . Plant impact on the biogeochemical cycle of silicon and related weathering processes I Basile-Doelsch , JD Meunier , C Parronm . Another continental pool in the terrestrial silicon cycle . Nature , 2005 . 433 ( 7024 ): 399 - 402 . 15674287 DOI: 10.1038/nature03217 http://doi.org/10.1038/nature03217 . Another continental pool in the terrestrial silicon cycle RA Berner . The rise of plants and their effect on weathering and atmospheric CO 2 . Science , 1997 . 276 ( 5312 ): 544 - 546 . DOI: 10.1126/science.276.5312.544 http://doi.org/10.1126/science.276.5312.544 . The rise of plants and their effect on weathering and atmospheric CO2 R Chen . Species of Bamboo and Their Planting and Using , 1984 . : Beijing Chinese Forestry Press , (in Chinese) . Species of Bamboo and Their Planting and Using WW Chen , ZJ Luo , F Chen , JW Lu , CP Ding . The nutrition status and nutrition diagnosis of bamboo leaves in the South of Hubei . Journal of Northeast Forestry University , 2004 . 32 ( 2 ): 41 - 44 . (in Chinese) . The nutrition status and nutrition diagnosis of bamboo leaves in the South of Hubei L Christanty , JP Kimmins , D Mailly . ‘Without bamboo, the land dies’: a conceptual model of the biogeochemical role of bamboo in an Indonesian agroforestry system . For Ecol Manage , 1997 . 91 ( 1 ): 83 - 91 . DOI: 10.1016/S0378-1127(96)03881-9 http://doi.org/10.1016/S0378-1127(96)03881-9 . ‘Without bamboo, the land dies’: a conceptual model of the biogeochemical role of bamboo in an Indonesian agroforestry system CL Dang , ZL Wu . Studies on the net primary production of Castanopsis orthacantha community . Journal of Yunnan University (Natural Sciences) , 1994 . 16 ( 3 ): 200 - 204 . (in Chinese) . Studies on the net primary production of Castanopsis orthacantha community NVJ de Bakker , MA Hemminga , J van Soelen . The relationship between silicon availability, and growth and silicon concentration of the salt marsh halophyte Spartina anglica . Plant and Soil , 1999 . 215 ( 1 ): 19 - 27 . DOI: 10.1023/A:1004751902074 http://doi.org/10.1023/A:1004751902074 . The relationship between silicon availability, and growth and silicon concentration of the salt marsh halophyte Spartina anglica LA Derry , AC Kurtz , K Ziegler , OA Chadwick . Biological control of terrestrial silica cycling and export fluxes to watersheds . Nature , 2005 . 433 ( 7027 ): 728 - 731 . 15716949 DOI: 10.1038/nature03299 http://doi.org/10.1038/nature03299 . Biological control of terrestrial silica cycling and export fluxes to watersheds E Epstein . The anomaly of silicon in plant biology . Proc Natl Acad Sci USA , 1994 . 91 ( 1 ): 11 - 17 . 11607449 DOI: 10.1073/pnas.91.1.11 http://doi.org/10.1073/pnas.91.1.11 . The anomaly of silicon in plant biology E Epstein . Silicon . Annu Rev Plant Physiol Plant Mol Biol , 1999 . 50 ( 1 ): 641 - 664 . 15012222 DOI: 10.1146/annurev.arplant.50.1.641 http://doi.org/10.1146/annurev.arplant.50.1.641 . Silicon XP Gao , CQ Zou , LJ Wang , FS Zhang . Silicon improves water use efficiency in maize plants . J Plant Nutr , 2004 . 27 ( 8 ): 1457 - 1470 . DOI: 10.1081/PLN-200025865 http://doi.org/10.1081/PLN-200025865 . Silicon improves water use efficiency in maize plants RE Graetz , JO Skjemstad . The Charcoal Sink of Biomass Burning on the Australian Continent . 2003 . : Victoria CSIRO , CSIRO Atmospheric Research Technical Paper No. 64 . The Charcoal Sink of Biomass Burning on the Australian Continent BT Hu , ZL Wang , SS Hong . Geographic distribution and content of available silicon in soils under Ph . pubescens stands in Zhejiang and Fujian Provinces . Forest Research , 1994 . 7 ( 4 ): 364 - 370 . (in Chinese) . Geographic distribution and content of available silicon in soils under Ph. pubescens stands in Zhejiang and Fujian Provinces PH Huang . Researches on the dynamic change of mineral nutrient elements in moso bamboo . Journal of Bamboo Research , 1983 . 2 ( 1 ): 87 - 111 . (in Chinese) . Researches on the dynamic change of mineral nutrient elements in moso bamboo YP Huang , XH Zhang . The Moso Bamboo , 1992 . : Xiamen Xiamen University Press , (in Chinese) . The Moso Bamboo QM Huang , DD Yang , YG Shen , GX Qiu . Studies on the primary productivity of bamboo ( Phyllostachys pubescens ) grove . Forest Research , 1993 . 6 ( 5 ): 536 - 540 . (in Chinese) . Studies on the primary productivity of bamboo (Phyllostachys pubescens) grove YX Jiang , JP Lu . Tropical Forest Ecosystems of Jianfengling in Hainan Island, China , 1991 . : Beijing Science Press , (in Chinese) . Tropical Forest Ecosystems of Jianfengling in Hainan Island, China PK Jiang , YW Yu . Nutrition elements contained in leafs of Phyllostachys praecox f. preveynalis and soil nutrients . Journal of Zhejiang Forestry College , 2000 . 17 ( 4 ): 360 - 363 . (in Chinese) . Nutrition elements contained in leafs of Phyllostachys praecox f. preveynalis and soil nutrients ZJ Li , P Lin . Accumulation and distribution of nutrient elements in Phyllostachys pubescens forest of south Fujian . Chinese Journal of Applied Ecology , 1995 . 6 ( Suppl. ): 9 - 13 . (in Chinese) . Accumulation and distribution of nutrient elements in Phyllostachys pubescens forest of south Fujian ZJ Li , P Lin , XZ Qiu . Studies on the biomass and productivity of Phyllostachys pubescens community in south Fujian . Journal of Xiamen University (Natural Science) , 1993 . 32 ( 6 ): 762 - 767 . (in Chinese) . Studies on the biomass and productivity of Phyllostachys pubescens community in south Fujian ZJ Li , JY He , YH Fang , 等 . P Lin . Study on Biological Cycle of Silicon Element in Moso Bamboo Community in Wuyishan Mountains . Wuyishan Research Series, Forest Ecosystem (1) , 1998 . : Xiamen Xiamen University Press , 153 - 157 . (in Chinese) . Study on Biological Cycle of Silicon Element in Moso Bamboo Community in Wuyishan Mountains ZJ Li , YM Lin , ZW Yang , P Lin . Accumulation and cycling of Ca and Mg in Castanopsis eyrei community in Wuyishan Mountains . Chinese Journal of Applied Ecology , 1998 . 9 ( 6 ): 592 - 596 . (in Chinese) . Accumulation and cycling of Ca and Mg in Castanopsis eyrei community in Wuyishan Mountains ZJ Li , CD Liu , ZW Yang , JY He , P Lin . Comparison of species diversity between closed and stable Castanopsis eyrei forests and Castanopsis eyrei forests with human disturbance in Mount Wuyi Nature Reserve . Journal of Phytoecology , 2000 . 24 ( 1 ): 64 - 68 . (in Chinese) . Comparison of species diversity between closed and stable Castanopsis eyrei forests and Castanopsis eyrei forests with human disturbance in Mount Wuyi Nature Reserve ZJ Li , XL Chen , HL Zheng . Ecology , 2004 . 2nd Ed : Beijing Science Press , (in Chinese) . Ecology YC Liang . Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress . Plant and Soil , 1999 . 209 ( 2 ): 217 - 224 . DOI: 10.1023/A:1004526604913 http://doi.org/10.1023/A:1004526604913 . Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress W Liese . Advances in bamboo research . Journal of Nanjing Forestry University , 2001 . 25 ( 4 ): 1 - 6 . . Advances in bamboo research P Lin . Phytocoenology , 1986 . : Shanghai Shanghai Science and Technology Press , (in Chinese) . Phytocoenology P Lin , QH Ye . Distribution and vegetation types of Huanggangshan in Wuyishan Mountains of Fujian, China . Braun-Blanquetia , 1993 . 8 56 - 69 . . Distribution and vegetation types of Huanggangshan in Wuyishan Mountains of Fujian, China YM Lin , P Lin , ZJ Li , JY He , CD Liu . Biomass and productivity of Castanopsis eyrei community in Wuyi Mountains . Journal of Xiamen University (Natural Science) , 1996 . 35 ( 2 ): 269 - 275 . (in Chinese) . Biomass and productivity of Castanopsis eyrei community in Wuyi Mountains YM Lin , ZJ Li , ZW Yang , P Lin , JY He , CD Liu . Accumulation and biological cycle of N and P elements in Castanopsis eyrei in Wuyi Mountains . Journal of Xiamen University (Natural Science) , 1997 . 36 ( 3 ): 460 - 465 . (in Chinese) . Accumulation and biological cycle of N and P elements in Castanopsis eyrei in Wuyi Mountains YM Lin , P Lin , ZJ Li , ZW Yang , CD Liu , JS Wang . Accumulation and biological cycle of K and Na elements in Castanopsis eyrei in Wuyi Mountains . Journal of Xiamen University (Natural Science) , 1998 . 37 ( 5 ): 283 - 288 . (in Chinese) . Accumulation and biological cycle of K and Na elements in Castanopsis eyrei in Wuyi Mountains XD Liu . The role of the silicate involved in community succession of the phytoplankton . Marine Environmental Science , 1996 . 15 ( 2 ): 38 - 43 . (in Chinese) . The role of the silicate involved in community succession of the phytoplankton WY Liu , SC Xie , KJ Xie . Nutrients accumulation and cycle on Lithocarpus xylocarpus community in North Part of Ailao Mountains, Yunnan, China . Acta Botanica Yunnanica , 1995 . 17 ( 2 ): 175 - 181 . (in Chinese) . Nutrients accumulation and cycle on Lithocarpus xylocarpus community in North Part of Ailao Mountains, Yunnan, China L Liu , XC Lin , AW Jin , TX Feng , CP Zhou , ZF Ji . Analysis of nutrient elements in various organs of Pleioblastus amarus . Journal of Zhejiang Forestry College , 2004 . 21 ( 2 ): 172 - 175 . (in Chinese) . Analysis of nutrient elements in various organs of Pleioblastus amarus JP Lu , ZM Wu . Phytochemistry characteristics of tropical forests in Jianfeng Mountains . Forest Research , 1991 . 4 ( 1 ): 1 - 9 . (in Chinese) . Phytochemistry characteristics of tropical forests in Jianfeng Mountains A Lux , M Luxová , J Abe , S Morita , S Inanaga . Silicification of bamboo ( Phyllostachys heterocycla Mitf.) root and leaf . Plant and Soil , 2003 . 255 ( 1 ): 85 - 91 . DOI: 10.1023/A:1026157424794 http://doi.org/10.1023/A:1026157424794 . Silicification of bamboo (Phyllostachys heterocycla Mitf.) root and leaf GT Miller . Environmental Science: Working with the Earth , 2001 . : Pacific Grove, California Brooks/Cole , . Environmental Science: Working with the Earth PK Nayar , AK Misra , S Patnaik . Evaluation of silica-supplying power of soils for growing rice . Plant and Soil , 1977 . 47 ( 2 ): 487 - 494 . DOI: 10.1007/BF00011505 http://doi.org/10.1007/BF00011505 . Evaluation of silica-supplying power of soils for growing rice DP Nie . The structure characteristics of bamboo groves in Dagangshan region, Jiangxi Province . Forest Research , 1992 . 5 693 - 699 . (in Chinese) . The structure characteristics of bamboo groves in Dagangshan region, Jiangxi Province ZQ Peng , YM Lin , JB Liu , XH Zhou , ZJ Guo , QR Guo , P Lin . Biomass structure and energy distribution of Phyllostachys heterocycla cv. pubescens population . Journal of Xiamen University (Natural Science) , 2002 . 41 579 - 583 . (in Chinese) . Biomass structure and energy distribution of Phyllostachys heterocycla cv. pubescens population CED Pereira , J Felcman . Correlation between five minerals and the healing effect of Brazilian medicinal plants . Biological Trace Element Research , 1998 . 65 ( 3 ): 251 - 259 . 9892497 . Correlation between five minerals and the healing effect of Brazilian medicinal plants JA Raven . Cycling silicon—the role of accumulation in plants . New Phytologist , 2003 . 158 ( 3 ): 419 - 430 . DOI: 10.1046/j.1469-8137.2003.00778.x http://doi.org/10.1046/j.1469-8137.2003.00778.x . Cycling silicon—the role of accumulation in plants N Stark , CF Jordan . Nutrient retention by the root mat of an Amazonian rainforest . Ecology , 1978 . 59 ( 3 ): 434 - 437 . DOI: 10.2307/1936571 http://doi.org/10.2307/1936571 . Nutrient retention by the root mat of an Amazonian rainforest HL Sun . Ecosystems of China , 2005 . : Beijing Science Press , (in Chinese) . Ecosystems of China E Takahashi , Y Miyake . Distribution of silica accumulator plants in the plant kingdom. (1) Monocotyledons . J Sci Soil Manure , 1976 . 47 296 - 300 . (in Japanese) . Distribution of silica accumulator plants in the plant kingdom. (1) Monocotyledons E Takahashi , T Tanaka , Y Miyake . Distribution of silicicolous plants in plant kingdom (5) . J Sci Soil Manure , 1981 . 52 503 - 510 . (in Japanese) . Distribution of silicicolous plants in plant kingdom (5) TT Wang . T Higuchi . The Above-Ground and Net Production of a Moso-Bamboo ( Phyllostachys pubescens ) Stand in Central Taiwan. Production and Utilization of Bamboos . 1981 . Proceedings of XVII IUFRO World Congress . Kyoto, Japan 125 - 130 . . The Above-Ground and Net Production of a Moso-Bamboo (Phyllostachys pubescens) Stand in Central Taiwan. Production and Utilization of Bamboos TH Wen . Evoluation on the factors of bamboo productivity . Journal of Bamboo Research , 1990 . 9 ( 2 ): 1 - 10 . (in Chinese) . Evoluation on the factors of bamboo productivity MD Winslow , K Okada , F Correa-Victoria . Silicon deficiency and the adaptation of tropical rice ecotypes . Plant and Soil , 1997 . 188 ( 2 ): 239 - 248 . DOI: 10.1023/A:1004298817861 http://doi.org/10.1023/A:1004298817861 . Silicon deficiency and the adaptation of tropical rice ecotypes GM Woodwell , RH Whittaker , RA Houghton . Nutrient concentrations in plant in Brookhaven Oak pine forest . Ecology , 1975 . 56 ( 2 ): 318 - 332 . DOI: 10.2307/1934963 http://doi.org/10.2307/1934963 . Nutrient concentrations in plant in Brookhaven Oak pine forest ZY Wu . Vegetation of China , 1980 . : Beijing Science Press , (in Chinese) . Vegetation of China QX Wu . Types and the forest structure of moso bamboo forests in Guizhou . Journal of Bamboo Research , 1983 . 2 ( 3 ): 112 - 124 . (in Chinese) . Types and the forest structure of moso bamboo forests in Guizhou CX Xu , ZP Liu , YL Liu . The physiological function of Silicon in plants . Communication on Plant Physiology , 2004 . 40 ( 6 ): 753 - 757 . (in Chinese) . The physiological function of Silicon in plants FC Zhou . Mathematical model of structure of moso bamboo forest . Research on Bamboos , 1987 . 6 ( 1 ): 1 - 31 . (in Chinese) . Mathematical model of structure of moso bamboo forest We thank Liu, C.D. and Liu, D.R. of Administrative Bureau of Wuyishan National Nature Reserve for field help, Tan, Bentio C. of National University of Singapore, Tang, J.J. of Zhejiang University, Chen, S.B. of Institute of Botany, the Chinese Academy of Sciences and anonymous reviewers who improved the manuscript with their comments. 10.1631/jzus.2006.B0849 Project (No. 30370275) supported by the National Natural Science Foundation of China 2006-03-27 2006-06-23 2006-10-17 2022-01-05 Copyright © 2006, Journal of Zhejiang University Science 2006 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 11 07