The reserve of weatherable primary silicates impacts the accumulation of biogenic silicon in volcanic ash soils
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- Henriet, C., De Jaeger, N., Dorel, M. et al. Biogeochemistry (2008) 90: 209. doi:10.1007/s10533-008-9245-0
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Banana plantlets (Musa acuminata cv Grande Naine) cultivated in hydroponics take up silicon proportionally to the concentration of Si in the nutrient solution (0–1.66 mM Si). Here we study the Si status of banana plantlets grown under controlled greenhouse conditions on five soils developed from andesitic volcanic ash, but differing in weathering stage. The mineralogical composition of soils was inferred from X-ray diffraction, elemental analysis and selective chemical/mineralogical extractions. With increasing weathering, the content of weatherable primary minerals decreased. Conversely, clay content increased and stable secondary minerals were increasingly dominant: gibbsite, Fe oxides, allophane, halloysite and kaolinite. The contents of biogenic Si in plant and soil were governed by the reserve of weatherable primary minerals. The largest concentrations of biogenic Si in plant (6.9–7 g kg−1) and soil (50–58 g kg−1) occurred in the least weathered soils, where total Si content was above 225 g kg−1. The lowest contents of biogenic Si in plant (2.8–4.3 g kg−1) and soil (8–31 g kg−1) occurred in the most weathered desilicated soils enriched with secondary oxides and clay minerals. Our data imply that soil weathering stage directly impacted the soil-to-plant transfer of silicon, and thereby the stock of biogenic Si in a soil–plant system involving a Si-accumulating plant. They further imply that soil type can influence the silicon soil–plant cycle and its hydrological output.
KeywordsSiliconMusaBiogenic SiWeatherable primary silicatesVolcanic ash soils
The global cycle of silicon receives increasing attention because Si has a crucial role in major biogeochemical processes such as the regulation of atmospheric CO2, nutrition of aquatic biota, and proton buffering through weathering (Sommer et al. 2006). It is being increasingly appreciated that terrestrial plants can exert a strong control on Si fluxes in the biogeosphere (Derry et al. 2005). Numerous plant species take up considerable quantities of H4SiO4 from soil solution (Raven 1983), which is carried from roots to transpiration sites through mass flow (Raven 2001) and active transport (Ma et al. 2006, 2007) and precipitates as biogenic opal (SiO2 · nH2O) called phytolith (Smithson 1956). Silicon is recycled into the soil from falling litter and decomposition of plant debris. A biogenic Si (BSi) pool is thus built up in both plant and soil compartments of terrestrial ecosystems (Alexandre et al. 1997; Markewitz and Richter 1998; Meunier et al. 1999). The soil BSi pool can be substantial, particularly in the humid tropics (10–40 g kg−1), and can be rapidly recycled (Alexandre et al. 1997; Cary et al. 2005). The soil–plant Si cycle is significant in comparison with weathering input and hydrologic output (Lucas et al. 1993; Alexandre et al. 1997; Markewitz and Richter 1998; Meunier et al. 1999), as most of the Si released to water streams can pass through the BSi pool (Derry et al. 2005). The building-up of that pool would primarily depend on the availability of H4SiO4 in the soil solution, which is controlled by silicate dissolution and clay formation in soil (Garrels 1967; Kittrick 1969), which both reflect soil constitution and weathering stage. The relationship between the soil mineral composition and Si soil-to-plant transfer is, however, poorly investigated though plant-BSi has been reported to vary depending on soil type (Fox et al. 1967; Berthelsen et al. 1999; Matichenkov et al. 2000; Schwandes et al. 2001). In humid tropical regions, weathering sequences of soils developed on volcanic ash are remarkably suited to study the impact of soil weathering stage on soil constitution and properties (Parfitt et al. 1983; Delvaux et al. 1989; Chorover et al. 1999; Chadwick et al. 2003), and on plant nutrient status (Delvaux et al. 1989; Chadwick et al. 1999). We have recently shown from a field study that soil weathering stage governs the leaf Si status in mature banana plants cultivated on soils derived from similar parent ash (Henriet et al. 2008). However, plant transpiration may have influenced the Si soil-to-plant transfer since climatic conditions were not homogeneous over the studied weathering sequence.
The objective of this study is twofold. Firstly, we assess the soil-to-plant transfer of Si by young banana plantlets (Musa acuminata cv Grande Naine) from soils developed on andesitic ash under controlled homogeneous greenhouse conditions. Secondly, we measure the BSi pool in soils. We further assess the link between the accumulation of BSi in plants and soil with the reserve of weatherable primary silicate minerals. We use banana plants to measure the availability of silicon since they take up Si proportionally to its concentration in the nutrient solution (0–1.66 mM Si: Henriet et al. 2006).
Materials and methods
Environmental and soil conditions
Soil type, mean annual rainfall (MAR) and elevation at each reference banana plot for each soil (Ws: Western slopes; Es: Eastern slopes)
Soil type (IUSS Working Group WRB 2006)
pH was measured in 5 g:25 ml soil:water suspensions (Page et al., 1982). Organic carbon content was determined according to the method of Walkley and Black (1934). Cation exchange capacity (CEC) and the content of exchangeable bases were determined according to Jackson (1965). Total elemental contents were measured by inductively coupled plasma/atomic emission spectrometry (ICP–AES) after fusion in Li-metaborate + Li-tetraborate at 1,000°C (Chao and Sanzolone 1992). Within a first set of selective extractions, dark oxalate-extractable (o), dithionite-citrate-bicarbonate (DCB) extractable (d) and pyrophosphate-extractable (p) contents of Si, Al and Fe were determined in the respective extracts by ICP–AES following the methods compiled in Dahlgren (1994). A second set of selective extractions was applied to address the pools of the so-called available Si (Sauer et al. 2006), by using the following extractants: (1) H2O extraction (adapted from Fox et al. 1967), (2) H2O extraction adapted here by adding flocculant SrCl2, (3) 0.01 M CaCl2 (adapted from Haysom and Chapman 1975), (4) 0.87 M acetic acid + 0.18 M Na acetate, buffered at pH4 (adapted from Imaizumi and Yoshida 1958), (5) 0.6 M citric acid + 0.4 M Na citrate, buffered at pH4 (adapted from Beckwith and Reeve 1963). The extraction procedure was standardised for all extractants as follows: a 5-g dry soil sample was placed into a 100 ml polyethylene cup with 50 ml extractant (soil:extractant ratio = 1:10) and shaken for 5 h at 20°C. The tubes were then centrifuged at 3,400g for 10 min and the supernatant was filtered through Whatman cellulose membrane (20–25 μm pore size). The concentrations of Si, Al, and Fe were determined by ICP–AES.
Soil particle-size analysis was achieved by quantitative recovery of clay (<2 μm), silt (2–50 μm) and sand (>50 μm) fractions after sonication and dispersion with Na+-saturated resins without any previous H2O2 oxidation of organic matter (Rouiller et al. 1972; Bartoli et al. 1991). This procedure is known for its great efficiency to disperse strongly micro-aggregated soils such as Andosols, Nitisols and Ferralsols (Bartoli et al. 1991; Delvaux et al. 1992; Pochet et al. 2007). Briefly, sand fractions were separated after ultrasonic dispersion of fine earth fraction (<2 mm) and repeated wet sieving. Clay and silt fractions were then collected and submitted to prolonged dispersion with Na+-resin. Clay was separated from silt by successive cycles of 24 h decanting and pipetting. The mineralogical composition was determined using X-ray diffraction (XRD) (Druker D8 Advance diffractometer). Prior to XRD, the clay and silt fractions were submitted to two successive treatments: H2O2 (6%, 40°C), and DCB extraction of residual free iron (Dahlgren 1994).
Soil biogenic Si (BSi) extraction and quantification
The five H2O2- and DCB-treated silt fractions (2–50 μm) were further submitted to an additional overnight dispersion (16 h) with Na+-saturated resins to avoid any clay contamination. Each silt fraction was divided into light (biogenic opal) and heavy components (other minerals), through a series of heavy liquid separations, using an aqueous zinc bromide (ZnBr2) solution with a density of 2.3 g cm−3 (adapted from Kelly 1990). Each silt fraction (2–5 g) was mixed with 20 ml of ZnBr2 and centrifuged at 3,400g for 10 min. After centrifugation, the supernatant containing the floating phytoliths was carefully and slowly removed with a pipette and collected in a glass vessel through a Teflon (polytetrafluoroethylene—PTFE) filter (2 μm) soaked with methanol. The sample was then remixed with 20 ml of ZnBr2 solution and again submitted to centrifugation at 3,400g for 10 min. The operation was repeated until the supernatant was clear. The filter was then abundantly rinsed with 1 M HCl, washed with distilled water, transferred with its opal load to a steel PTFE-lined pressure vessel, with 15 ml of 0.5 M NaOH, and placed overnight in an oven at 150°C. After cooling, the NaOH solution was filtered into a 25 ml polyethylene volumetric flask (Herbauts et al. 1994). Si and Al in solution were determined by ICP–AES and expressed on a soil dry matter basis at 105°C. Considering the selective floating process and the specific NaOH dissolution of opal in sediments (Ragueneau et al. 2005), the Si measured by ICP–AES corresponds to the BSi content in the silt fraction. As no method is currently available to determine BSi in the clay fraction, that Si content represents the minimum value of soil BSi content. Indeed, though this method selectively dissolves BSi, it does not extract it quantitatively (Saccone et al. 2007).
We used young banana plantlets (Musa acuminata cv Grande Naine, AAA group, Cavendish, dessert banana) issued from tissue culture, and produced in nutrient medium devoid of silicon. A total of 150 plantlets were weaned in a nursery under controlled conditions also devoid of any Si supply. Seventy homogeneous plantlets with an average height of 9.5 cm were selected: 10 per soil for the pot experiment, and four per soil for biomass correction (see below). Ten plantlets were stored after weaning and dried at 60°C for 1 week for further elemental analysis to assess the Si concentration of initial plant materials.
The experimental design involved five soils (Table 1) and 10 replicates per soil, consisting of 50 individual banana plantlets. Each plantlet was planted in a 2 l plastic pot containing a known soil mass depending on soil bulk density (620–1,300 g dry weight). Nitrogen (N), phosphorus (P2O5), and potassium (K2O) were applied at amounts of 0.4, 0.3, and 1 g pot−1, respectively. Nemathorin® (1 g pot−1) was used to prevent nematode attack. The soil was covered by an inert black plastic sheet to avoid weed development and limit direct evaporation. The soil moisture content was adjusted at field capacity: (1) each pot, including soil and plant was weighted to determine the reference pot weight at field capacity; (2) three times a week, each pot was weighted, and distilled water was supplied to reach the reference pot weight; daily plant transpiration was deduced; (3) every 3 weeks, the reference pot weight was corrected by measuring the fresh biomass of one plant per soil. The pot experiment was conducted for 84 days in a greenhouse with a global radiance of 8.25 MJ m−2 (day:night ~12 h:12 h), 83.4% mean relative humidity, and 23.8°C mean temperature. Once a week, the numbers of totally and partially unfurled leaves were measured (Carlier et al. 2002), the length (l) and width (w) of the unfurled leaves. The leaf surface area (LA) was computed from the equation LA = 0.7 × l × w (Rufyikiri et al. 2000).
Plant growth, transpiration and Si concentration
Averages of growth parameters and cumulated transpiration calculated for each soil at the end of the experiment (n = 10)
Cumulated leaf areaa (cm²)
Shoot dry matter (g)
Cumulated transpirationb (g)
Si concentration in banana plant parts, balanced Si concentration and quantity of Si exported in banana shoot (aerial parts excluding roots), and quantity of Si exported with respect to the cumulated transpiration (Si:transpiration ratio: mg Si per kg of water transpired) (n = 10)
Si concentration in various organs (g kg−1 DM)
Balanced Si conc. in shoot (g kg−1 DM)
Quantity of Si in shoot (mg pot−1)
Si:transpiration ratio (mg kg−1)
y[M + P]
Although this experiment has been conducted under controlled homogeneous greenhouse conditions, plant growth parameters differed among the five soils, with lower average values of shoot dry matter and cumulated leaf area in Es-Ni and Ws-An. These differences result from physical constraints to root development at the beginning of the experiment leading to delayed plant growth. Lower cumulated leaf area and shoot dry matter thus induced lower cumulated transpiration in Es-Ni and Ws-An, which may have interfered with the Si status of banana plants. We thus expressed the quantity of Si exported in banana shoot relative to cumulated transpiration for further comparison between soils (Table 3). This parameter defines the Si:transpiration ratio, and is expressed in mg Si per kg of water readily transpired by plant.
Physical and chemical properties of soils
Major soil properties, as measured in the fine earth (<2 mm): pH, organic carbon content (Corg), exchangeable cations, cation exchange capacity (CEC), and particle-size distribution
Exchangeable bases (cmolc kg−1)
CEC (cmolc kg−1)
Particle-size analysis (%)
Total element contents and selective extractions
Total elemental contents (t) and total reserve in bases (TRB)
Total elemental contents (t) and Si, Al and Fe contents in oxalate (o), dithionite (d) and pyrophosphate (p) extracts
Minerals detected by X-ray diffraction in the clay fraction (<2 μm) of soils
Soil BSi content
Soil biogenic Si (BSi) content and Al impurities as extracted by NaOH (0.5 M) in the silt fraction (2–50 μm) after densimetric separation
NaOH-extractable elements (g kg−1)
Al/Si atomic ratio
Quantity of soil BSi (g pot−1)
Si, Al and Fe extracted from soils
Average extractable contents of elements (from 2 replicates of each soil) for the various selective extractants
Extractable soil elements (mg kg−1)
Na citrate pH4
Na Acetate pH4
H2O + SrCl2
CaCl2 (0.01 M)
Si gradient in the banana plant
Soil weathering stage and mineralogical properties
Contents of extractable silicon in soils
The extractable Si content decreases in the sequence Na citrate pH4 > Na acetate pH4 > H2O ≥ CaCl2 = (H2O + SrCl2) (Table 9). Only the CaCl2-, (H2O + SrCl2)- and acid Na acetate-extractable Si contents follow a similar trend in that they clearly differ between Ws- and Es-soils with the largest values in the former. The pH values of the CaCl2, H2O, and (H2O + SrCl2) extracts range between 5.5 and 6. The CaCl2 solution is recognised to extract the aqueous Si fraction (Haysom and Chapman 1975) and to provide a measure of readily available Si (Chapman et al. 1981; Berthelsen et al. 2001). H2O extraction induces the dispersion of clay minerals in Es-Ni, Es-Fe and Ws-Ca, as suggested by the relatively large values of H2O-extractable Si, and by the values of the atomic Si/(Al + Fe) ratio ranging between 1 and 1.3, characteristic for clay fractions dominated by 1:1 phyllosilicates. Considering the similar contents of CaCl2- and (H2O + SrCl2)-extractable Si in soils, we conclude that water-soluble Si is extracted by both extractants, CaCl2 and SrCl2 acting as flocculent. The acid buffered Na acetate extracted 3-5 times more Si than CaCl2 and (H2O + SrCl2). This extractant is recognised to mobilise the labile Si from soils (Sauer et al. 2006). As an acid buffer, it partially dissolves weatherable minerals, and extracts substantial amounts of Al, invariably larger than Si in all soils, except in Ws-Ca. The Na citrate-extractable Si contents are the largest, as compared to the Si contents measured in the other extractants (Table 9). They are particularly high in the Andosols, where the acid Na citrate extraction likely promotes mineral dissolution, because of the ability of citrate to complex Al and Fe from amorphous constituents, as suggested by the correlation between oxalate- and Na citrate-extractable contents of Al (r = 0.91) and Si (r = 0.83) (Tables 6 and 9).
Silicon bioavailability and soil weathering stage
Soil weathering stage impacts the BSi pool in the soil–plant system
The soil BSi content in the soils used in this experiment (8–58 g kg−1) corresponds to the range reported so far in tropical environments (9–40 g kg−1) (Alexandre et al. 1997; Cary et al. 2005). These soil BSi contents are 10–20 times larger than in soils under temperate climates (Wilding and Drees 1971). The relatively large soil BSi pool in tropical soils results from warm and wet climatic conditions promoting the rapid recycling of silicon in the soil–plant system (Drees et al. 1989; Conley et al. 2006). The above-ground standing vegetation also plays an important role in the BSi content in soil: the soil BSi production of a rainforest in Congo ranges from 58 to 76 kg ha−1 year−1 (Alexandre et al. 1997).
The contribution of plants to the Si continental reservoir can be significant (Alexandre et al. 1997). The annual BSi production by plants at global scale indeed ranges between 60 and 200 Tmol year−1 (Conley 2002) and rivals that produced by diatoms in the oceanic biogeochemical cycle (240 Tmol year−1) (Tréguer et al. 1995). Moreover, plant-BSi is recycled into the soil from falling litter in a separate soil–plant Si cycle that can be significant in comparison with weathering input and hydrologic output (Derry et al. 2005). Consequently, as already stated by Conley (2002), consideration must be given to the influence of the terrestrial BSi pool on variations in the global biogeochemical Si cycle over different times scales. The results presented here and in our previous study (Henriet et al. 2008) show that soil mineralogical composition, and more generally soil weathering stage and soil development, can strongly influence the bioavailability of silicon for plant uptake, and hence the building-up of the terrestrial BSi pool. We thus believe that more consideration should be given to soils as major sink-source actors in the soil–plant Si cycle to further study the mobility of Si at continental scale, better understand Si export to water streams, and thus better assess Si mass balances at watershed scale.
We have studied the soil-to-plant transfer of Si using young banana plants cultivated in controlled greenhouse conditions, on volcanic ash soils differing in mineralogical composition, weathering stage and soil development. The largest concentrations of biogenic Si in plant (6.9–7 g kg−1) and soil (50–58 g kg−1) occur in the least weathered soils, where total soil Si content is above 225 g kg−1. The lowest contents of biogenic Si in plant (2.8–4.3 g kg−1) and soil (8–31 g kg−1) occur in the most weathered desilicated soils enriched with secondary oxides and clay minerals, where total soil Si content is below 185 g kg−1. These experimental data obtained in controlled conditions are strongly consistent with those acquired in the framework of a large scale topsoil-foliar survey carried out in mature banana fields (Henriet et al. 2008). These data indicate that silicon availability is positively influenced by the reserve of easily weatherable primary minerals, and thus more generally by soil weathering stage and soil development. We conclude that soil weathering stage impacts the soil-to-plant transfer of Si, and thereby the stock of biogenic Si in a soil–plant system involving a Si-accumulating plant. Our data further suggest that soil type can influence the silicon soil–plant cycle and its hydrological output. We thus believe that more consideration should be given to soils as key sink-source actors in the Si soil–plant cycle at watershed and continental scales.
We are grateful to L. Bodarwé, A. Iserentant and C. Givron for their strong analytical and technical support, X. Draye for fruitful discussions (UCL), and T. Drouet de la Thibauderie (ULB, Belgium) for the loan of the PTFE-lined pressure vessels. We thank the reviewers and the Associate Editor for their constructive comments and attractive suggestions. C·H. is supported by the “Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture” (FRIA) of Belgium, and S·O. by the “Fonds National de la Recherche Scientifique” (FNRS) of Belgium. This research was supported by the FNRS research convention N°2.4629.05 and by the “Fonds Spécial de Recherche” (FSR) 2005 of the UCL.