Lignin, carbohydrate, and amino sugar distribution and transformation in the tropical highland soils of northern Thailand under cabbage cultivation, Pinus reforestation, secondary forest, and primary forest.
Soil organic matter (SOM) encompasses plant, animal, and microbial residues in all stages of decomposition and it is often closely associated with inorganic soil components. The cycling of SOM is strongly dependent on the microbial environment, which is influenced by soil temperature, moisture, and vegetation. Despite intensive research on this issue, there are still many open questions concerning the highly complex structure and the transformation of SOM. Since the availability of nutrients and the formation of stable soil aggregates are closely related to SOM, advancing our knowledge about the topic is a prerequisite for a sustainable soil management.
The major C input into forest soils is holocellulose (cellulose and hemicellulose), which makes up approximately half of the dry weight of leaves (Haider 1992). Plant-derived sugars, especially pentose polymers, serve as the major source of energy and C for soil microorganisms. Microorganisms synthesise primarily hexose polymers and release them into the soil (Murayama 1984; Oades 1984). Both the concentrations and compositions of saccharides can, therefore, be used to assess the plant-microbe relationship in SOM dynamics. However, they cannot provide information about the microbial origin of organic substrates in the soil (Zhang et al. 1997). Different amino sugars derive from different groups of soil microorganisms (Sowden and Ivarson 1974; Parson 1981; Zhang et al. 1998). Hence, the amounts of hexosamines and muramic acid and their ratios (glucosamine to galactosamine and glucosamine to muramic acid) can serve as useful indicators for bacterial and fungal contribution to SOM (Zhang et al. 1998; Amelung et al. 1999a).
Lignin decomposes slowly and represents a recalcitrant fraction in soil and litter (Haider 1992). During decomposition of lignin, intramolecular bonds between phenylpropanoid components of the lignin are cleaved and oxidised, and phenolic derivatives are released (Chen and Chang 1982). The ratio of acid to aldehyde of phenolic moieties can be used to estimate the extent of lignin biotransformation (Hedges and Ertel 1982).
Most of the investigations on composition and transformation processes of SOM were conducted on soils in temperate regions and tropical lowlands (e.g. Kogel-Knabner et al. 1988a; Guggenberger et al. 1994). Although extensive research on the storage and turnover of SOM (Torn et al. 1997) as well as on the function of SOM pools in nutrient cycling has been undertaken in the tropical mountain regions (Townsend et al. 1995), few studies addressed the chemical structures and their transformation (Guggenberger and Zech 1999; Solomon et al. 2000). Therefore, this study focussed on the undulating highlands of northern Thailand, a region rapidly deforested and intensively cultivated in the past decades.
Since the end of the 1980s, parts of that region were reforested, whereas wide areas were still subject to intensive agriculture, resulting in pronounced losses of soil organic matter. The re-establishment of forests is expected to induce a build-up of soil organic matter in the long term. Thus, these hills offer a range of soils with soil organic matter in various states of transformation, which allows the transformation of C species under tropical conditions to be studied (Townsend et al. 1995).
The objectives of our study were (i) to examine the composition and distribution of lignin, amino sugars, and carbohydrates as revealed by alkaline CuO oxidation and hydrochloric acid and trifluoroacetic acid hydrolyses, respectively; and (ii) to evaluate the transformation of chemical structures of carbon during the decomposition of SOM under tropical conditions along a decomposition gradient within a given site (depth profiles) and between sites (different management systems). For this purpose, we compared wet chemical analyses of lignin, amino sugars, and neutral sugars of bulk soils and alkaline soil extracts with the previously published [sup.13]C-NMR signature of alkaline-extractable SOM of the study sites (Moller et al. 2000).
Materials and methods
Site description and sampling
Experimental sites were on the Khun Sathan Research Station, which is located in the Na Noi district of northern Thailand at an elevation of 1350-1500 m (17[degrees]48'N, 100[degrees]35'E). The mean annual temperature was 25[degrees]C, and the average annual rainfall was about 1400 mm with a dry season from December to April. Four representative ecosystems of the region were investigated: 20-year-old Pinus kesiya (Royle ex Gordon) reforestation, secondary forest (15 years old) mixed with a 15-year-old Pinus kesiya (Royle ex Gordon) reforestation, primary forest, and cabbage cultivation sites. The soils, Dystric and Humic Cambisols on lower slopes and Skeletic Umbrisols and Lithic Leptosols on steeper sloping areas, derived from shale and sandstone. Under the forest vegetation, organic layers covered the mineral soil surface. The forest floor beneath the primary forest was mull-type, whereas at the Pinus reforestation and the secondary forest moder-type forest layers were found. The chemical properties of the soils at the 4 study sites are given in Table 1. Kaolinite and illite were the dominant clay minerals in the soils. The bulk density of the mineral soils was almost uniform and ranged from 1.6 g/[cm.sup.3] in the topsoils to 1.8 g/[cm.sup.3] in the subsoils. The average bulk density of the organic layers was 0.02 g/[cm.sup.3] under the primary forest, 0.03 g/[cm.sup.3] under the secondary forest, and 0.06 g/[cm.sup.3] under the reforestation. At all forest sites, the vegetation rooted mostly in the upper 30 cm of the mineral soil; below 30 cm depth only very few roots were found. A more detailed description of the sites and soils is given in Moller et al. (2000, 2002).
Soils were sampled in autumn 1997 and spring 1998. For each plot, 2 representative soil profiles were selected and sampled by horizons. Additionally, from 3 subplots all across each of the 4 sites, composite samples of O, A, and B horizons were collected from small soil pits using a radial sampling scheme (Wilding 1985). Per subplot, 7 subsamples of 200 [cm.sup.3] of the entire organic layer and of 100 [cm.sup.3] of the mineral soil were collected and thoroughly mixed. Samples of the A horizons were taken from 0-10 cm depth and samples of the B horizons were from 30-40 cm depth. Transformation states of SOM were studied by using the first set of samples, while the latter served to examine land-use and vegetation effects. All samples were air-dried and the mineral samples were sieved to <2 mm.
The organic C and total N contents were analysed on ground subsamples with a CHNS-analyser (Vario EL, Elementar Analysensysteme GmbH, Hanau, Germany). Inorganic N was extracted from the soils using 2 M KCl and the extracts were analysed colorimetrically for N[O.sub.3.sup.-] and N[H.sub.4.sup.+] (SAN Plus, Skalar Analytical B.V., Breda, The Netherlands). Organic N was calculated by the difference of total and inorganic N. Despite illite being the second abundant clay mineral in the studied soils, the only detectable inorganic N form was N[O.sub.3.sup.-], except for the topsoil horizons of the fertilised cabbage cultivation and the organic forest floor layers where N[H.sub.4.sup.+] comprised up to 20% of the total N. Nitrate represented between 5% (topsoil) and 55% (subsoils) of the total N.
The extraction of alkaline-soluble SOM was done according to the procedure of Schnitzer (1982), modified by Sumann et al. (1998). The soil samples were extracted 3 times with a solution containing 0.1 M NaOH and 0.4 M NaF at a ratio of soil to extraction solution of 1:5 (w/v). The extracts were dialysed (molecular weight cutoff, MWCO, 12 000-14 000 daltons) in order to remove salts, then freeze-dried. The yields of extracted C were 14-23% in the organic forest foot layers and 19-39% in the mineral soil horizons (Moller et al. 2000).
The amount of lignin and its state of oxidative decomposition in bulk soils and freeze-dried alkaline-extractable SOM was estimated using the analyses of lignin-derived phenols after alkaline CuO oxidation at 170[degrees]C for 2 h (Hedges and Ertel 1982). Ethylvanillin was added as an internal standard before CuO oxidation and phenylacetic acid before derivatisation in order to determine the recovery of ethylvanillin. C- 18 (Mallinckrodt Baker Corp., Phillipsburg, NJ, USA) served as filling material for solid phase extraction of the phenolic oxidation products (Kogel 1986). Phenols were eluted and derivatised with a 1 : 1 mixture of pyridine and N,O-bis(trimethysilyl)-trifluoroacetamide. The trimethylsilyl derivatives were analysed by capillary gas-liquid chromatography. The determination was done on an HP 6890 gas chromatograph (Agilent Technologies, Inc., Palo Alto, CA, USA), equipped with an FID detector and utilising an HP Ultra 2 fused silica column (Agilent Technologies, Inc., Palo Alto, CA, USA) of 25 m length.
The sum of vanillyl (V), syringyl (S), and cinnamyl (C) phenols released from the lignin macromolecules by CuO oxidation was used to estimate the lignin content of the sample, the VSC-lignin. Absolute lignin contents cannot be determined (Amelung et al. 1999b). The mass ratios of acid to aldehyde forms of vanillyl units [[(ac/al).sub.V]] and of syringyl to vanillyl units (S/V) were taken to assign the degree of microbial alteration of lignin within the sample.
Determination of neutral sugars and uronic acids was conducted according to the method of Amelung et al. (1996). Individual neutral and acidic sugars were released from non-cellulosic carbohydrates with 4 M trifluoroacetic acid (TFA) at 105[degrees]C for 4 h. The hydrolysates were filtered through glass fiber filters and dried using a rotary evaporator. The samples were purified by percolation through XAD-7 (Rohm and Haas Co., Philadelphia, PA, USA) and Dowex 50W X8 (Dow Chemical Co., Midland, MI, USA) resin. The resulting hexoses, pentoses, and uronic acids were converted to O-methyloxime trimethylsilyl derivatives (Andrews 1989) and separated by gas-liquid chromatography using an HP 5 fused silica column (Agilent Technologies, Inc., Palo Alto, CA, USA) of 25 m length. Separated compounds were detected by flame ionisation. Myo-inositol was added as internal standard prior to hydrolysis, and 3-O-methylglucose was added prior to the derivatisation in order to estimate the recovery of myo-inositol.
Amino sugars, i.e. glucosamine, galactosamine, mannosamine, and muramic acid were determined according to the method of Zhang and Amelung (1996). Samples of bulk soils and freeze-dried alkaline-extractable SOM were hydrolysed with 6 M HCl at 105[degrees]C for 8 h, then the hydrolysates were filtered and neutralised. After freeze-drying, the residues were re-dissolved in methanol, and the resulting solutions were dried again in an air stream and then derivatised to aldononitrile acetates. Before hydrolysis, myo-inositol was added as the first internal standard. Identification and quantification of amino sugars was conducted by capillary gas-liquid chromatography using an HP 5 fused silica column (Agilent Technologies, Inc., Palo Alto, CA, USA) of 25 m length. 3-O-methylglucose was used as a recovery standard.
Means of concentrations of VSC-lignin, carbohydrates, amino sugars, organic C, and N of the whole data set were compared by horizons among the 4 experimental sites using 1-way analyses of variance (ANOVA), followed by a post-hoc separation (significant at P = 0.05) of means done by the univariate l.s.d, test. The Pearson product moment correlation with a 2-tailed test of significance was used to examine the relationships between VSC-lignin, carbohydrates, amino sugars, organic C, and N in bulk soil and in alkaline-extractable SOM and between [sup.13]C-NMR spectral areas obtained on alkaline-extractable SOM. The statistical analyses were conducted using the software package STATISTICA 5.0 for Windows.
Results and discussion
Organic carbon and organic nitrogen
The sites showed comparable decreases in organic C and organic N with soil depth (Fig. 1, Table 2). The content of organic C ranged from 340 to 470 g/kg in organic horizons of the forest floor layers, from 27 to 72 g/kg in topsoil horizons, and down to 3 g/kg in the deeper subsoil of the primary forest. Organic N ranged from 17 g/kg in organic forest floor layers to < 1 g/kg in the subsoil horizons. The primary forest showed the highest organic C and N concentrations in the topsoil (65 [+ or -] 9 g OC/kg, 4.2 [+ or -] 0.5 g ON/kg, respectively), compared with the significantly lower contents at the cabbage cultivation and the reforestation sites (41 [+ or -] 7 g OC/kg, 2.7 [+ or -] 0.3 g ON/kg; 40 [+ or -] 4 g OC/kg, 2.8 [+ or -] 0.3 g ON/kg, respectively).
The replacement of forests by arable land at the reforestation and cabbage cultivation sites about 30 years ago induced a significant net loss of SOM, expressed by 40% lower C and 25% lower N concentrations in the mineral soil compared with the primary forest site. Since the use of N fertilisers at the cabbage cultivation site did not start before 1995, the depletion in N is still detectable. All other sites have never received fertilisers. Reforestation with Pinus following 20 years of cultivation did not lead to a build-up of organic matter in the mineral soil; rather an organic forest floor layer developed from litter that was not incorporated into the mineral soil. This reflects the recalcitrant nature of the Pinus needle litter at the reforestation site with high contents of substances more resistant to decomposition like lignin, waxes, or phenols (Oades 1988; Zech et al. 1997). Additionally, the organic layer of the reforestation site had a wider ratio of organic C to organic N than the other organic forest floor layers (Fig. 1, Table 2), which may inhibit the break-up of plant materials and decrease the rate of decomposition (Troeh and Thompson 1993). The little organic matter in the mineral soil under the reforestation could also result from little input of root litter and root exudates since the trees were young and a ground vegetation was almost missing. Compared with species of the ground vegetation, trees release only a small amount of dead roots per year (Troeh and Thompson 1993).
The low amounts of SOM present in the mineral soil of the reforestation, therefore, may still be derived from the previous primary forest vegetation. This agrees with the findings of Vitorello et al. (1989), Desjardins et al. (1993), and Boutton et al. (1998), who documented vegetation changes by [delta][sup.13]C analyses. They found a high proportion of SOM originating from the native forest vegetation remaining in soil following deforestation and long-term pasture.
The topsoils of all sites showed ratios of organic C to organic N >14. With increasing soil depth, the ratios of organic C to organic N in most soils changed to values around 8-10. Even compared with the ratios of organic C to total N reported for mineral soil horizons of acidic temperate and tropical forest soils (e.g. Post et al. 1985; Stevenson 1986; Zech et al. 1992), the values found here were small, maybe because of rapid recycling of nitrogen at the study sites.
Lignin compounds and transformation in the forest floor litter and mineral soil
Lignin-derived phenols (VSC) in the organic layer increased in the order primary forest < secondary forest < reforestation (Fig. 2) with double the amount in the needle litter (52.5 g/kg C) compared with the deciduous primary forest (25.4 g/kg C). Generally, needle litter seems to be richer in lignin than non-skleromorphic broad-leaved litter (e.g. Kogel 1986). Our results accord with these findings.
[FIGURE 2 OMITTED]
The different quality of organic layers under the vegetation types corresponded to a strong decrease in the ratio of syringyl to vanillyl units (S/V) in the order primary forest > secondary forest > reforestation (Fig. 2). Values were close to zero at the reforestation site, which is due to the inherently lower proportion of syringyl units in gymnosperm lignin (Sarkanen and Ludwig 1971).
The ratio of acid to aldehyde forms of the vanillyl units [[(ac/al).sub.V]] is indicative of the degree of side-chain oxidation in the lignin molecule, because cleavage of C[alpha]-C[beta] and/or oxidation of C[alpha] bonds by white-rot fungi leads to an increased production of phenolic acids with respect to the aldehydes obtained from CuO oxidation (Zech and Kogel-Knabner 1994). The (ac/al)v ratio did not show any significant difference in the organic layers of the forested sites. However, the ratio of VSC to N decreased significantly in the order reforestation > secondary forest > primary forest in the organic and in the A horizons (Table 3). Haider (1992) stated that C pools in plant residues have turnover rates according to their ratio of VSC to N. A decreasing ratio of VSC to N accelerates the decomposition of the individual C pools.
From the surface to the uppermost subsoil horizons, the VSC-lignin showed a progressive decrease (Fig. 3). The extent of this decrease was the same at all four sites (Figs 2 and 3). Due to the influence of root litter and partial mineralisation of easily degradable organic matter, i.e. carbohydrates (see beneath), we found an increase of VSC in all Oe horizons. At the secondary forest site the decrease with soil depth was less steep due to the shallow soil at this site as indicated by the relatively high VSC content in the CA horizon compared with the A horizon. In the deeper subsoil horizons, VSC remained almost constant with depth. This points to a decreased rate of degradation possibly because of lignin-degrading fungi being less active in the subsoil or because of stabilisation of partly degraded lignin compounds by sorptive interactions with soil minerals (Baldock and Skjemstad 2000; Kaiser and Guggenberger 2000).
[FIGURE 3 OMITTED]
Some subsoil horizons, e.g. the C (profile A) and the Bw3 (Profile B) under the reforestation exhibited increased yields of CuO oxidation products compared with the overlying horizons. This possibly resulted from translocation processes of water-soluble organic matter. Chemically altered, polymeric, water-soluble lignin fragments produced during microbial degradation of lignin (Ellwardt et al. 1981; Seelenfreund et al. 1990) or water-soluble compounds of other sources are possibly leached into the subsoil and stabilised there through adsorption at sesquioxides or clay minerals (Baldock and Skjemstad 2000; Kaiser and Guggenberger 2000).
For the angiosperm lignin under the primary forest, the syringyl structures in the litter were preferentially degraded as indicated by a decrease of the S/V ratio from the surface down to the A horizon, while the [(ac/al).sub.V] ratio increased. Simultaneously the relative intensity of signals of aromatic and phenolic C in liquid-state [sup.13]C-NMR spectra of alkaline extracts of these soils decreased and that of carbonyl C increased (Moller et al. 2000). According to Kogel-Knabner et al. (1988a) and Zech and Kogel-Knabner (1994), increases in carboxyl C and decreasing proportions of aromatic C and C-normalised yields of CuO oxidation products with soil depth are characteristic of decomposition and transformation processes in O and A horizons.
In summary, the most pronounced increase in lignin alteration appeared at the transition between the organic layer and the upper mineral soil, whereas lignin in the mineral subsoil either seemed to degrade slower or was replenished by translocation of less degraded organic matter from the upper soil compartments.
Polysaccharides are the major component of forest litter (Zech and Kogel-Knabner 1994). They comprise cellulose, a crystalline polymer of glucose, which is not digestible through TFA, and hemicellulose composed of various pentoses and hexoses. Therefore, monomeric sugars released by acid hydrolysis with TFA originate only from plant-derived hemicellulose and microbial metabolites. The total concentrations of non-cellulosic carbohydrates (neutral as well as acid sugars) fit in the range of the concentrations of non-cellulosic carbohydrates reported by e.g. Kogel-Knabner et al. (1988b) for organic layers (182-318 g/kg C) and by Guggenberger et al. (1994) and Solomon et al. (2000) for mineral soils (87-188 g/kg C). The concentrations of non-cellulosic carbohydrates in the organic layers of the forest sites increased significantly in the order primary, forest < secondary forest < reforestation (Fig. 4). Non-cellulosic carbohydrates decreased from the organic layer to the A horizon by 20, 17, and 44% at the primary forest, the secondary forest, and the reforestation, respectively (Fig. 4). In the A and B horizons, the differences in the non-cellulosic carbohydrate concentrations of the sites were less pronounced, but the concentrations at the primary forest were lower than those of the reforestation.
[FIGURE 4 OMITTED]
Hempfling et al. (1987) and Kogel-Knabner et al. (1988a) reported that, due to microbial metabolisation of carbohydrates, the depletion of non-cellulosic carbohydrates was less pronounced than the losses of cellulose in forest soil, which decreased with depth from 20-25% of organic C in the organic layer to <3% in the A horizon. The contribution of microbial-derived saccharides to the carbohydrate composition of soil can he estimated using quotients of sugar monomers because microorganisms synthesise little if any pentoses, while the pentoses xylose and arabinose are ubiquitous constituents of plant cells (Oades 1984). Therefore, the higher the ratio of hexoses to pentoses [(galactose + mannose)/(arabinose + xylose)], the greater the microbial contribution to the soil carbohydrate fraction (Oades 1984). In addition, Murayama (1984) attributed increasing ratios of deoxy hexoses to pentoses [(fucose + rhamnose)/(arabinose + xylose)] to microbial production of deoxy sugars. These ratios increased strongly from the organic layer down to the A horizons, showing the increasing proportion of microbial-derived polysaccharides in the carbohydrate fraction (Figs 4 and 5) with enhanced organic matter decomposition.
With increasing soil depth, the ratios of hexoses to pentoses as well as the concentrations of neutral sugars and uronic acids did not show a clear trend (Fig. 5). The carbohydrate concentrations varied throughout all mineral soil profiles and the ratios of hexoses to pentoses at the primary and secondary forests and the cabbage cultivation were almost constant.
An interesting irregularity was observed at the Bw3 and Bw4 horizon of profile A of the primary forest, as it was also found for the lignin pattern. The Bw3 horizon showed a minimum of non-cellulosic carbohydrates with low ratios of hexoses to pentoses. In contrast, the underlying Bw4 horizon represented a maximum of non-cellulosic carbohydrates and had higher ratios of hexoses to pentoses. This finding suggests the input of relatively fresh material. Because the root density in the 2 subsoil horizons was low, we assume that the input was through organic matter translocation by percolation or interflow and subsequent sorption to the mineral matrix in the Bw4 horizon. This assumption was supported by the [sup.13]C-NMR spectra of extractable organic matter in this horizon showing a maximum in O-alkyl C and a minimum in carbonyl C (Moller et al. 2000). The translocation is probably followed by a stabilisation and protection against further mineralisation through bindings at sesquioxides and clay minerals in the subsoil (Baldock and Skjemstad 2000; Kaiser and Guggenberger 2000). The leaching of carbohydrates may be another possible explanation for the high carbohydrate concentrations in the subsoil horizons as compared with the topsoils.
Significantly higher (P < 0.05) total concentrations of amino sugars were found in the A horizon of the reforestation than the primary and secondary forest and the cabbage cultivation (Fig. 6). The higher amino sugar concentrations may be attributed to a decreased mineralisation of hexosamines and muramic acid due to more recalcitrant litter and/or to increased contribution of microbial substances at the reforestation site as indicated by the presence of visible fungal hyphae, coupled with an increasing population of bacteria living upon the residues of fungi (Troeh and Thompson 1993).
[FIGURE 6 OMITTED]
The amino sugar contents in soil organic matter increased with soil depth (Fig. 7), indicating increasing contribution of microbe-derived compounds. This can be induced by progressive decay of plant-derived organic matter and subsequent build-up of secondary products by the degrading microorganisms. It may also be due to preferential leaching of lysed bacterial cell material compared with other water-soluble organic compounds (Moller et al. 2000). Amino and amide-N groups are considered to add to bonding interactions in clay-organic complexes (Lowe 1983). Therefore, microbial compounds such as amino sugars once produced may accumulate through stabilisation by clay particles in soil. The ratios of amino sugar-N to total N increased in the order primary forest < secondary forest < reforestation and were within the range of values compiled by Kelley and Stevenson (1996).
[FIGURE 7 OMITTED]
Glucosamine is an important constituent of the fungal cell wall, while in terrestrial ecosystems muramic acid uniquely originates from bacteria (Kenne and Lindburg 1983). Sowden and Ivarson (1974) demonstrated that little if any galactosamine is synthesised by fungi during fungi-inoculated incubation experiments. Hence, the ratios of glucosamine to galactosamine (GluN/GalN) and glucosamine to muramic acid (GluN/Mur) were used to assess the fate of bacteria and fungi-derived organic matter. Because galactosamine is not only a component of mucopolysaccharides but more abundant in animals (Amelung 2001), the GluN/Mur ratio seems more suitable to distinguish between bacterial and fungal influence on the composition of SOM.
Interpretation of the amino sugar ratios is difficult since the turnover times of the amino sugars may differ. Glucosamine seems to be more stable than galactosamine and muramic acid, because it occurs in recalcitrant glomaline, a glycoprotein produced in the soil by arbuscular mycorrhizal fungi (Wright and Upadhyaya 1996). Nevertheless, ratios of amino sugars have been used to trace the microbial origin of the amino sugar-N in soil (Sowden and Ivarson 1974; Kogel and Bochter 1985; Zhang and Amelung 1996) and may be used to determine the changing microbial environment in the long-term (Guggenberger et al. 1999) and along degradation gradients in soil profiles.
The patterns of amino sugars were considerably influenced by vegetation and land use. For the organic layers, the GluN/Mur ratio decreased in the order primary forest > secondary forest > reforestation (Fig. 6). This indicates that the proportions of fungi-derived amino sugars were largest at the primary forest and smallest at the reforestation sites. The decrease of the GluN/Mur ratios from the organic layers to the mineral soil (Figs 6 and 7) suggests decreasing contribution of fungi-derived amino sugars with the increasing transformation of SOM in the mineral soil.
Structural composition of SOM
The chemical transformation of C structures during the decomposition of organic matter was examined by comparing wet chemical analyses of lignin, amino sugars, and neutral sugars of bulk soils and alkaline-extractable organic matter with the liquid-state [sup.13]C-NMR signature (presented in Moller et al. 2000) of the alkaline-extractable organic matter.
We found similar results for VSC and amino sugars for the bulk soil samples (Figs 3 and 7) and the alkaline-extractable organic matter (Figs 8 and 9). The correlation between bulk soil samples and alkaline-extractable organic matter for the sum of CuO oxidation products and the amino sugars were highly significant (R = 0.97 and 0.92, respectively, Table 4), indicating that the alkaline extracts were representative for VSC and the sum of amino sugars.
[FIGURES 8-9 OMITTED]
Concerning the individual CuO oxidation products there were almost no differences between the alkaline extracts and the bulk soil samples. The alkaline-extractable organic matter showed higher ratios of acid to aldehyde forms of the vanillyl units than the bulk samples (Figs 3 and 8). This suggests that lignin at an increased degree of decomposition is easier extractable than the remaining lignin, possibly due to destruction of macromolecules and oxidative formation of functional groups. However, the results of the alkaline extracts and the bulk soil samples showed the same trends, with only few exceptions concerning the subsoil of the cabbage cultivation and the primary forest.
Also for the individual amino sugars, there were almost no differences (Figs 7 and 9). Muramic acid was over-represented in the alkaline extracts of the subsoil horizons, whereas glucosamine seemed to be more under-represented. This agrees with higher GluN/Mur ratios in the bulk soil compared with the alkaline-extractable organic matter. Muramic acid, similar to other organic compounds having carboxyl functional groups (Oades et al. 1989), sorbs strongly to mineral particles (Kaiser et al. 1997). Therefore, the preferential alkaline extractability of muramic acid compared with the other amino sugars may result from desorption from sesquioxides and clay minerals.
Neutral sugars in alkaline-extractable organic matter and bulk soil samples were weakly correlated (R = 0.67), and for uronic acids no correlation was found (Figs 5 and 10). Thus, the alkaline extracts seemed not to be representative of uronic acid content or distribution. The individual neutral sugars in the bulk soil samples as well as the alkaline extracts fluctuated within the soil profiles. However, the ratios of hexoses to pentoses in bulk soil samples and alkaline extracts showed similar trends with increasing soil depth. This suggests that the alkaline extracts were partially representative for the bulk soil samples.
[FIGURES 5 & 10 OMITTED]
To elucidate the relationship and dynamics of different C species as identified by different approaches, we compared the concentrations of VSC, amino sugars, and neutral sugars identified by wet chemical methods with chemical shift regions assessed by liquid-state [sup.13]C NMR (Table 5). We found significant correlations for VSC with phenolic C (R = 0.74) and for amino sugars with O-alkyl C (R = 0.67) for the forest sites bulk samples (without the gleyic horizons of the primary forest), whereas the neutral sugars did not show any clear correlation. The parallel decrease of VSC and of the signal intensity of phenolic C suggests that most of the phenolic C has to be attributed to lignin. The lack of correlation between wet-chemically determined neutral sugars and O-alkyl C is likely to be due to the used method, which does not extract sugar monomers from cellulose.
Concerning amino sugars and O-alkyl C, closer correlations were found when dividing the profiles into the organic layers and the mineral soil horizons (Fig. 11). In the organic layers, a significant negative correlation was found ([R.sup.2] = 0.74). The negative correlation can be attributed to the preferential mineralisation of plant-derived carbohydrates (Zech et al. 1997), compared with a slower rate of remetabolised microbial products such as amino sugars.
[FIGURE 11 OMITTED]
In contrast, the amino sugar contents and O-alkyl C in the mineral soil horizons were positively correlated ([R.sup.2] = 0.86) at a highly significant level, suggesting changed SOM dynamics compared with the organic layer. In the mineral soil we found more or less constant concentrations of non-cellulosic carbohydrates with increasing depth, but strongly increasing amino sugar concentrations. Thus, the enrichment of O-alkyl C may partly be the result of bacterial resynthesis (Moller et al. 2000) coupled with a high production of amino sugars and a stabilisation of these microbial products by adsorption to clay minerals and sesquioxides. This agrees with the assumption of Baldock et al. (1992) that organic matter sorbed to sesquioxides is dominated by aliphatic and O-alkyl constituents. Another explanation for the increase in O-alkyl C is a relative enrichment of cellulose with depth due to the decay of lignin. Because cellulose is labile compared with lignin, it is not likely that the decrease in lignin with depth exceeds that of cellulose. However, since we did not determine cellulose, we cannot rule out a preferential mineralisation of lignin. Nevertheless, it seems reasonable to conclude that besides a possible relative enrichment of cellulose the amino sugars contribute largely to the increasing proportion of O-alkyl C with depth.
Summary and conclusions
The aim of this investigation was to study the chemical transformation of SOC structures during the decomposition of SOM under tropical conditions, using wet chemical analyses of lignin, amino sugars, and neutral sugars of bulk soil samples and alkaline soil extracts and to compare these results with the liquid-state [sup.13]C-NMR signature presented in Moller et al. (2000). The replacement of forests by arable land at the reforestation and cabbage cultivation sites resulted in enhanced breakdown of soil organic matter. However, 20 years of Pinus growth did not lead to a build-up of organic matter in the mineral soil, suggesting that the remaining SOM in the mineral soil of the reforestation was, at least partly, derived from the previous primary forest vegetation. The profiles of the forest plots provide natural systems that allow to follow the long-term course of SOM transformation, showing the typical pattern of decomposition expressed by the higher degree of side chain oxidation, increasing carboxyl functionality, and the decrease in VSC and aromatic compounds with increasing soil depth. The results also point to a predominantly fungal decomposition in the organic layer, changing to a decomposition dominated by bacteria with soil depth, as indicated by increasing concentrations of amino sugars, narrower OC-to-ON ratios, and decrease in plant-derived carbohydrates. On condition that alkaline extracts are representative for bulk soil samples, it is possible to compare the results obtained from the wet chemical analyses with liquid-state [sup.13]C-NMR signatures. This applied to VSC, amino sugars and, with some limitations, to neutral sugars, but not to uronic acids. We found significant correlations for VSC with phenolic C and for amino sugars with O-alkyl C for the bulk forest site samples, whereas the neutral sugars did not show any clear correlation. Therefore, we concluded that most of the phenolic C signal intensity is attributed to lignin in these soils and that the enrichment of O-alkyl C with increasing soil depth is a result of increased bacterial resynthesis. Consequently, bacterial amino sugars contributed largely to the increase of O-alkyl C.
Table 1. Selected chemical properties of the investigated soils Data from Moller et al. (2002). Samples were by horizons from 2 soil profiles per site and from several small soil pits (composite O, A, and B horizons) all over the respective sites. N, number of samples; [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII], soil pH measured potentiometrically in 0.01 M Ca[Cl.sub.2] at a soil-to-solution ratio of 1:2.5 (w/v); CEC, cation exchange capacity as determined with 1 M N[H.sub.4]OAc (pH = 7.0) according to Avery and Bascomb (1974); Clay, soil clay content determined by the pipette method (Avery and Bascomb 1974); [Al.sub.o], [Fe.sub.o], acid oxalate-extractable Al and Fe determined with acid 0.2 M ammonium oxalate at pH 3 (Schwertmann 1964); [Fe.sub.d], dithionite-extractable Fe determined by the sodium dithionite-citrate-bicarbonate method (Mehra and Jackson 1960) Soil compartment N [MATHEMATICAL CEC EXPRESSION NOT (mmol/kg) REPRODUCIBLE IN ASCII] Pinus reforestation (Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) Organic horizons 7 4.8 [+ or -] 0.3 384 [+ or -] 150 A horizons 5 4.8 [+ or -] 0.4 154 [+ or -] 60 B and C horizons 9 4.6 [+ or -] 0.6 103 [+ or -] 34 Secondary forest (Humic Cambisols-Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) Organic horizons 6 5.6 [+ or -] 0.5 396 [+ or -] 90 A horizons 5 4.6 [+ or -] 0.5 209 [+ or -] 86 B and C horizons 7 4.3 [+ or -] 0.3 137 [+ or -] 78 Primary forest (Humic Cambisols) Organic horizons 6 5.1 [+ or -] 0.4 420 [+ or -] 33 A horizons 5 3.8 [+ or -] 0.1 253 [+ or -] 114 B and C horizons 15 4.2 [+ or -] 0.2 110 [+ or -] 60 Cabbage cultivation (Humic Cambisols-Dystric Cambisols- Skeletic Umbrisols-Lithic Leptosols) A horizons 6 4.7 [+ or -] 0.4 181 [+ or -] 33 B and C horizons 10 4.4 [+ or -] 0.2 126 [+ or -] 44 Soil compartment Clay [Al.sub.o] (g/kg) Pinus reforestation (Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) Organic horizons n.d. n.d. A horizons 401 [+ or -] 111 3.8 [+ or -] 0.5 B and C horizons 392 [+ or -] 87 2.2 [+ or -] 0.6 Secondary forest (Humic Cambisols-Dystric Cambisols- Skeletic Umbrisols-Lithic Leptosols) Organic horizons n.d. n.d. A horizons 370 [+ or -] 224 4.5 [+ or -] 0.9 B and C horizons 330 [+ or -] 207 3.1 [+ or -] 1.3 Primary forest (Humic Cambisols) Organic horizons n.d. n.d. A horizons 533 [+ or -] 63 6.3 [+ or -] 0.7 B and C horizons 472 [+ or -] 68 2.5 [+ or -] 1.5 Cabbage cultivation (Humic Cambisols-Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) A horizons 479 [+ or -] 42 4.4 [+ or -] 1.2 B and C horizons 402 [+ or -] 70 4.4 [+ or -] 1.7 Soil compartment [Fe.sub.o] [Fe.sub.d] (g/kg) Pinus reforestation (Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) Organic horizons n.d. n.d. A horizons 6.2 [+ or -] 0.3 25 [+ or -] 6 B and C horizons 4.2 [+ or -] 1.3 29 [+ or -] 9 Secondary forest (Humic Cambisols-Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) Organic horizons n.d. n.d. A horizons 7.8 [+ or -] 1.8 29 [+ or -] 10 B and C horizons 5.8 [+ or -] 1.9 31 [+ or -] 12 Primary forest (Humic Cambisols) Organic horizons n.d. n.d. A horizons 12.8 [+ or -] 1.4 38 [+ or -] 7 B and C horizons 5.1 [+ or -] 1.9 35 [+ or -] 11 Cabbage cultivation (Humic Cambisols-Dystric Cambisols-Skeletic Umbrisols-Lithic Leptosols) A horizons 7.2 [+ or -] 0.7 22 [+ or -] 7 B and C horizons 6.5 [+ or -] 1.1 25 [+ or -] 9 n.d., not determined. Table 2. Organic carbon and organic nitrogen concentrations in the fine-earth fraction (<2 mm) of the investigated soil profiles OC data of the profile set A taken from Moller et al. (2000). OC, organic carbon; ON, organic nitrogen Horizon Profile A Depth OC ON OC/ON (cm) (g/kg) Reforestation Dystric Cambisol Oi 4-2 465 11.1 42 Oe 2-0 365 11.8 31 A 0-15 41 2.8 15 Bw 15-38 10 0.9 11 CB 38-65 7 0.7 10 C 65+ 7 0.7 10 Secondary forest Skeletic Umbrisol Oi 1.5-0.5 452 12.5 36 Oe 0.5-0 346 10.5 33 A 0-23 48 2.9 15 CA 23-36 27 2.0 13 C 36+ 13 1.1 12 Primary forest Humic Cambisol Oi 2-0 458 16.7 27 A 0-23 67 4.5 15 BA 23-40 21 1.8 12 Bw1 40-62 9 0.9 10 Bw2 62-90 5 0.5 10 Bw3 90-112 4 0.5 8 Bw4 112-128 3 0.4 8 Bg1 128-155 3 0.4 8 Bg2 155+ 5 0.5 10 Cabbage cultivation Dystric Cambisol A 0-20 45 3.1 15 AB 20-38 20 1.7 12 Bw1 38-70 11 1.1 10 Bw2 70-120+ 7 0.8 9 Horizon Profile B Depth OC ON OC/ON (cm) (g/kg) Reforestation Dystric Cambisol Oi 2.5-1.5 471 11.2 42 Oe 1.5-0 393 10.4 38 A 0-24 38 3.0 14 Bw1 24-56 11 1.0 11 Bw2 56-83 8 0.7 11 Bw3 83-110+ 4 0.4 10 Secondary forest Humic Cambisol Oi 0.5-0 455 11.0 41 A 0-32 68 4.6 15 AB 32-55 40 3.1 13 CB 55-70+ 10 0.9 11 Primary forest Humic Cambisol Oi 1-0.5 470 15.3 31 Oe 0.5-0 439 18.9 23 A 0-30 79 5.0 16 Bw1 30-57 14 1.1 13 Bw2 57-70 14 1.1 13 BC 70-90 9 0.8 11 C 90+ 5 0.4 12 Cabbage cultivation Dystric Cambisol A 0-20 29 2.7 15 BA 20-40 11 0.9 12 Bw1 40-60 5 0.5 10 Bw2 65+ 4 0.4 10 Table 3. Ratios of lignin-derived phenols (VSC) to total N (g/g) of composite samples Primary Secondary Refores- Cabbage forest forest tation cultivation Organic layer 0.76 0.81 1.94 -- A horizons (0-10 cm) 0.07 0.13 0.18 0.12 B horizons (30-40 cm) 0.04 0.09 0.05 0.07 Table 4. Correlations (Pearson R) between wet chemical analyses of the bulk soil samples and the NaOH extracts of forest soil profiles A Bulk samples NaOH extracts VSC Amino sugars Neutral sugars VSC 0.97 *** -0.87 *** 0.70 ** Amino sugars -0.81 *** 0.92 *** -0.82 *** Neutral sugars 0.76 *** -0.66 ** 0.67 ** Uronic acids -0.16 0.36 -0.11 Bulk samples NaOH extracts Uronic acids VSC 0.30 Amino sugars -0.38 Neutral sugars 0.35 Uronic acids 0.24 * P < 0.05; ** P < 0.01; *** P < 0.001; n = 19. Table 5. Correlations between the wet chemical analyses of bulk soil samples and spectral regions of solution [sup.13]C NMR of NaOH extracts of forest soil profiles A Results of [sup.13]C-NMR spectroscopy on NaOH extracts were taken from Moller et al. (2000) Carbonyl C Phenolic C Aromatic C VSC -0.53 * 0.74 *** 0.38 Amino sugars 0.32 -0.81 *** -0.62 ** Neutral sugars -0.67 ** 0.49 * 0.21 O-alkyl C Methoxyl C Alkyl C VSC -0.45 0.57 ** 0.38 Amino sugars 0.67 ** -0.31 -0.25 Neutral sugars -0.25 0.45 0.49 * * P < 0.05; ** P < 0.01; *** P < 0.001; n = 19.
This project was financially supported by the Deutsche Forschungsgemeinschaft (DFG Ze 154/47-1), the International Board for Soil Research and Management (IBSRAM) and the German Academic Exchange Service (DAAD). We are indebted to all the people of the IBSRAM, especially Suraphol Chandrapatya and Jean-Pierre Bricquet, for the help concerning the organisation of the field work. We thank the Royal Forest Department (RFD) of Thailand for allowing us to carry out the research at the Khun Sathan RFD Station. Especially we are grateful to Warin Jirasuktaveekul, chief of Watershed Research Division at the Royal Forest Department, Bangkok. For the help during the sampling we thank the former chief of the Khun Sathan station, Montree Puthawong, and the staff at Khun Sathan, Ed, Mr Mai and all others. This study would not have been possible without the help of Nualsri Kanchanakool, former head of the Soil Analyses Division at the Land Development Department in Bangkok, and of Chalinee Niamskul, UI-Consulting, Bangkok. Tanja Gonter and Andre Wetzel assisted in the analyses of the samples. The manuscript profited greatly from the competent and constructive suggestions of two anonymous referees and the critical comments of Ludwig Haumaier, Georg Guggenberger, and Wulf Amelung.
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Manuscript received 4 April 2001, accepted 27 March 2002
A. Moller (A), K. Kaiser (A B), and W. Zech (A)
(A) Institute of Soil Science and Soil Geography, University of Bayreuth, 95440 Bayreuth, Germany.
(B) Corresponding author; email: firstname.lastname@example.org
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|Author:||Moller, A; Kaiser, K.; Zech, W.|
|Publication:||Australian Journal of Soil Research|
|Date:||Nov 1, 2002|
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