Eur J Forest Res (2004) 123: 177–188 DOI 10.1007/s10342-004-0025-7
O R I GI N A L P A P E R
Klaus Lorenz Æ Caroline M. Preston Æ Susan Krumrei Karl-Heinz Feger
Decomposition of needle/leaf litter from Scots pine, black cherry, common oak and European beech at a conurbation forest site
Received: 5 February 2004 / Accepted: 7 May 2004 / Published online: 3 July 2004 Springer-Verlag 2004
Abstract Litter decomposition was studied for 2 years in a mixed forest serving as a water protection area (RhineNeckar conurbation, SW Germany). Two experiments differing in initial dry weight equivalent in litterbags were set up: one to compare decomposition of European beech leaves (Fagus sylvatica) with common oak leaves (Quercus robur), and the other comparing decomposition of Scots pine needles (Pinus sylvestris) with black cherry leaves (Prunus serotina Ehrh.), respectively. Mass losses were greater for oak litter than for beech (75.0 versus 34.6%), and for cherry litter than for pine (94.6 versus 68.3%). In both experiments, a strong initial loss of soluble compounds occurred. The changes in litter N and P concentrations and the decrease in C-to-N ratio coincided with changes in residual mass. However, neither tannin and phenolic concentrations nor NMR could explain the pronounced variation in mass loss after 2 years. Differences in litter palatability and toughness, nutrient contents and other organic compounds may be responsible for the considerable differences in residual mass between litter types. The fast decay of black cherry leaves appears to play a major role in the present humus dynamics at the studied site. Since black cherry has a high N demand, which is mainly met by root uptake from the forest floor, this species is crucial for internal N cycling at this conurbation forest K. Lorenz (&) Æ S. Krumrei Institut fu¨r Bodenkunde und Standortslehre, Universita¨t Hohenheim, Emil-Wolff-Str. 27, 70599 Stuttgart, Germany E-mail:
[email protected] Tel.: +49-711-4593669 Fax: +49-711-4593117 C. M. Preston Pacific Forestry Centre, Natural Resources Canada, 506 West Burnside Rd., Victoria, BC, V8Z 1M5, Canada S. Krumrei Æ K.-H. Feger Institut fu¨r Bodenkunde und Standortslehre, Technische Universita¨t Dresden, Pienner Str. 19, 01735 Tharandt, Germany
site. These effects together may significantly contribute to prevent nitrate leaching from the forest ecosystem which is subject to a continuous N deposition on an elevated level. Keywords Litter quality Æ 13C CPMAS NMR spectroscopy Æ Nutrient cycling Æ Nitrogen retention
Introduction Forest soils in conurbation regions can accumulate nutrients (notably nitrogen, phosphorus) but also heavy metals and other pollutants originating from atmospheric deposition (Lovett et al. 2000; Pouyat et al. 2002; Pouyat and McDonell 1991). Few studies have reported effects of the urban environment on soils in adjacent forests. Significantly affected were the soil fungal community, decomposers, litter decomposition rates, net nitrification rates and soil carbon pools and fluxes (Baxter et al. 2002; Goldman et al. 1995; Markkola et al. 2002; Pouyat and McDonell 1991; Pouyat et al. 1997; Zhu and Carreiro 1999). Forests in conurbation areas often play a prominent role for public drinking water supply from groundwater (Dudley and Stolton 2003). Hence, such forests require special attention in order to protect related functions of the soil as filter, buffer, and transformer. Notably the transformations of organic matter in the top soil are crucial in preventing a release of nitrate and other potential pollutants into the hydrosphere. Exotic plants are often introduced into conurbation forests for ornamental reasons (Pouyat et al. 2002). For example, during the first half of the 20th century, the North American species black cherry (Prunus serotina Ehrh.) was introduced to forests in Germany. There were multiple motivations, but fire protection, insect control and site amelioration were the most prominent (cf. Starfinger 1990; Haag und Wilhelm 1998). However, black cherry grows fast and shrubby, increasingly
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hampering silvicultural operations, notably the re-introduction of European beech and common oak beneath the pine canopy. On the positive side, cherry litter decomposes quickly, thereby improving soil quality by promoting the decay of mor humus layers and an increase in soil pH (von Wendorff 1952). Furthermore, black cherry accumulates nutrients, in particular N, K, Ca and Mg (Feger et al. 2003). Due its superiority in competition on poor sites with sandy soils, Prunus serotina is now widely spread in Germany with the main focus in the lowlands of N Germany and the upper Rhine valley (SW Germany) (Meersschaut et al. 1999; Starfinger 1990). Forestry practice, however, regards black cherry as a weed that should be removed to ensure growth and performance of the dominant trees and to allow the re-introduction of natural deciduous species (notably beech and oak) under the canopy of conifers (cf. Haag and Wilhelm 1998). So far there is no evidence demonstrating negative effects of such removal measures. The biodegradation of plant litter is greatly influenced by its chemical characteristics (Almendros et al. 2000). Initial litter N and P contents are often positively correlated with early decay rates (Berg 2000; Vesterdal 1999). Negative correlations between initial polyphenol contents and rates of decomposition have been reported (Loranger et al. 2002; Palm and Sanchez 1991). The rate of nutrient cycling can also be reduced by tannins, which amount up to 20% of the plant dry weight (Ha¨ttenschwiler and Vitousek 2000; Kraus et al. 2003b; Northup et al. 1998; Preston 1999; Yu and Dahlgren 2000). Determination of C fractions in litter by solid-state 13C nuclear magnetic resonance (NMR) spectroscopy has proven useful in characterizing litters with respect to their potential to decompose and release nutrients. In particular, the content of alkyl C (waxes and cutin), as determined by NMR, increases during decomposition. Cutin is highly resistant to decomposition and is related to physical toughness (Gallardo and Merino 1993; Preston et al. 1997). Therefore the content of alkyl C may be a useful indicator of litter decomposability (Baldock and Preston 1995). Identification of litter characteristics that are consistently closely related to decomposability has proven surprisingly difficult. Across a broad range of litter types, the C-to-N ratio appears to be the best predictor of decay rate (Enriquez et al. 1993; Pe´rez-Harguindeguy et al. 2000). The litterbag method has been used frequently in many decomposition studies (Swift et al. 1979). In comparison with mini-container, cotton-strip, 15N, 14C, 13 C isotopes and bait-lamina methods, all relevant biological, microbiological, chemical and physical measurement endpoints for the determination of organic matter (OM) breakdown could be applied for the litterbag method (Knacker et al. 2003). However, the litterbag method has also several disadvantages; e.g. its robustness has not been studied systematically, but the method has been taken for granted by scientists. Furthermore, a systematic approach to studying its
reproducibility has not yet been undertaken, and no interlaboratory comparison or ring test has been carried out. Other OM (e.g. roots, fungal hyphae) might enter the litterbags during exposure in the field and hamper the interpretation of changes in C, N, P and K concentrations. However, despite the disadvantages, the litterbag method at present is the most appropriate technique available to study OM breakdown in decomposition studies under field conditions (Knacker et al. 2003). We followed decomposition over 2 years in two litterbag studies in a conurbation forest in Germany. One experiment was set up with leaf litter from two deciduous species, European beech (Fagus sylvatica) and common oak (Quercus robur), and the second with needle and leaf litter from Scots pine (Pinus sylvestris) and black cherry (Prunus serotina Ehrh.), respectively. In addition to changes in litter mass and concentrations of C, N and P, we characterized litter samples using specific analyses for condensed tannins (CT) and polyphenols, and solid-state 13C nuclear magnetic resonance spectroscopy with cross-polarization and magic angle spinning.
Materials and methods Study site Litter decomposition was studied in the MannheimKa¨fertal forest, located in the Rhine-Neckar conurbation very close to the city of Mannheim (northern upper Rhine valley, SW Germany, Table 1). It is a vast forest area which is of major importance for the public Table 1 Site properties of the study area (Ries et al. 2000; Feger et al. 2001, 2003) Easting 3464988 Northing 5490800 Elevation 88 m a.s.l. Mean annual temperaturea 10.6 C Annual precipitationa 659 mm Parent material Aeolian sand covering Rhine terrace Soil profile (FAO) Dystric Cambisol Humus type (Mull)-moder pH (H2O) Of 4.4 Oh 4.0 0–5 cm 3.9 5–10 cm 4.0 Present atmospheric deposition Nitrogen 25 kg ha 1 year 1 Sulphur 10 kg ha 1 year 1 b Tree species Overstorey: 100% Pinus sylvestris Understorey: 60% Prunus serotina 20%Fagus sylvatica 10% Quercus robur 10% Tilia cordata Stand age 70–100 years a Averages (30-year), meteorological station Mannheim-Mu¨hlschleuse (Schirmer und Vent-Schmidt 1979) b Haag und Wilhelm (1998)
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drinking water supply for 0.5 million people. The climate is warm and relatively dry. Soil pH is very low even in the subsoil. However, due to an elevated rate of atmospheric N deposition, humus forms are relatively favorable (mull-moder types) and appear to have improved during recent decades (Krumrei et al. 2003). The stand consists of ca. 90-year-old Scots pine (Pinus sylvestris), whereas black cherry (Prunus serotina) forms a second layer which is very dense. Therefore, other deciduous species (notably beech and oak), despite being promoted by forest management during recent decades, form only a minor portion of the understorey. Nutrition of pine shows suboptimal supply with N and slight tendencies for disharmonies with respect to P and K (Feger et al. 2003). The deposition history in the conurbation is clearly reflected in elevated pools of N, S and heavy metals (Ries et al. 2000). Litter preparation and sampling In November 1999, freshly fallen senescent leaves from beech (Fagus sylvatica), oak (Quercus robur), black cherry (Prunus serotina Ehrh.) and brown needles from pine (Pinus sylvestris) were collected by hand and nets beneath mature trees at the study site. Two litterbag experiments were set up, one to compare the decomposition of beech versus oak leaves, and the other to compare pine needles with black cherry leaves. Beech and oak litter (5 g dry weight equivalent) and 2.5 g of cherry and pine litter were put into polyester-net litterbags (12·12 cm; 1 mm mesh), respectively. In November 1999, 35 bags of each litter were pinned to the forest floor surface in 7 blocks (0.5 m2). From each of these blocks, 7 litterbags were collected in May 2000 (after 0.5 years) and November 2001 (after 2 years), respectively. Litterbags were handsorted to remove mesofauna and external debris. Litter aliquots from each bag were dried at 70 C to constant mass and weighed for calculation of mass loss. For the proanthocyanidin and Folin Ciocalteu assays and for chemical analysis, dried composite samples for each species and date of collection were ground in a Wiley mill. Analysis of C, N, and P Total C and N concentrations of ground litters were analysed in duplicate by oxidative flash combustion using a Vario EL Foss Heraeus. Total phosphorus concentrations were determined in duplicate in extracts after wet digestion with HNO3 using a AES-ICP Spectro Ciros CCD. Proanthocyanidin (PA) assay The procedure was modified slightly from those reported previously (Lorenz et al. 2000). A standard solution (0.5 mg ml 1 in methanol) was prepared using purified
condensed tannin from the needles of black spruce (Picea mariana (Mill.) B.S.P.) (Lorenz and Preston 2002). Litter samples were analysed in two stages to determine extractable and residual tannins. Extraction was performed twice by adding acetone/water (70:30) (v/ v), and the extracts were combined. The insoluble residue was air dried for analysis of residual tannins. Sample concentrations were determined from the calibration curve established for black spruce tannin. Total tannin was expressed as the sum of extractable and residual tannin. The response in the assay depends on the proanthocyanidin:prodelphinidin ratio of the tannin, hence tannin concentrations should be regarded relative to the tannin standard (Kraus et al. 2003a). Folin Ciocalteu assay The procedure was modified slightly from those reported previously (Preston et al. 1997; Preston 1999). The reagent, prepared each day, was 20% (w/v) sodium carbonate solution. A stock solution (0.1 mg ml 1 in water) was prepared using a pure catechol (k 1480, Sigma). Sample concentrations in the combined acetone/ water extracts of the proanthocyanidin assay were determined from the absorbances of prepared catechol standards at 750 nm. Concentrations of phenolics should be regarded relative to the standard catechol. However, purifying standards from the same litter material would be helpful for the interpretation of sample absorbances (Appel et al. 2001). The Folin Ciocalteu method provides a broad measure of all readily oxidized compounds including tannins, non-tannin phenolics and non-phenolic compounds (Schofield et al. 1998). 13
C CPMAS NMR spectroscopy
Solid-state 13C NMR spectra of litter with cross-polarization and magic-angle spinning (CPMAS NMR) were obtained using a Bruker MSL 300 spectrometer (Bruker Instruments Inc., Karlsruhe, Germany) operating at 75.47 MHz. Dry, powdered samples were spun at 4.7 kHz in a 7-mm OD rotor. Spectra were acquired with 1 ms contact time, 2 s recycle time, and 6,000 scans, and were processed using 30–40 Hz line-broadening and baseline correction. Chemical shifts are reported relative to tetramethylsilane (TMS) at 0 ppm, with the reference frequency set using adamantane. Dipolar dephased (DD) spectra were generated by inserting a delay period of 40–50 ls without 1H decoupling between the crosspolarization and acquisition portions of the CPMAS pulse sequence. All DD spectra were obtained using the TOSS sequence for Total Suppression of Spinning Sidebands. The NMR spectra of litters were divided into chemical shift regions as follows: 0–50 ppm, alkyl C; 50–60 ppm, methoxyl C; 60–93 ppm, O-alkyl C; 93–112 ppm, di-O-alkyl C and some aromatics; 112–
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140 ppm, aromatic C; 140–165 ppm, phenolic C; and 165–190 ppm, carboxyl C. Boundaries were adjusted slightly to correspond with spectral minima. Areas of the chemical shift regions were determined after integration and expressed as percentages of total area (‘‘relative intensity’’). There are limitations in the quantitative reliability of CPMAS spectra, but it is appropriate to use them to compare intensity distributions among similar samples (Preston et al. 1994, 1997). The DD spectra were used only for qualitative discussion. Difference spectra (2-year minus initial spectra) were used to get an impression of the nature of the more resistant C structures accumulating during decomposition. These were obtained by subtracting the initial from the 2-year spectra, using the MSL software. In this qualitative procedure, the heights of the largest peaks were matched (mainly the O-alkyl signal), and then the 2-year spectrum subtracted. Small adjustments were made in the height of the 2-year spectrum to generate a difference spectrum that best maintained overall phasing and minimized distortion, in the eyes of the operator. Statistical analysis Values for remaining mass are based on arithmetic means (±standard deviation) of the 7 samples collected after 0.5 and 2 years of exposition. For statistical validity of the results, the nonparametric Mann-Whitney U-test (Sachs 1978) was applied to compare pairwise two means (beech/oak, pine/cherry). The significance level of 95% was used. Comparison of mean values was performed with the statistical program package SPSS. The tannin, total phenolics and elemental analyses were carried out on composite samples and are interpreted qualitatively.
Results Mass, chemical and biochemical changes Litter mass remaining after 0.5 and 2 years of decomposition are given in Table 2. Remaining mass after 0.5 years ranged from 31.7–85.5%, and was significantly lower for oak litter than for beech, and for cherry litter than for pine. These differences persisted for the second sampling, with only 5.4% of initial mass remaining for Table 2 Remaining mass during litter decomposition, n=7a
cherry, while 31.7% of the initial mass was still remaining for pine. After 2 years, the remaining mass for oak litter was also significantly lower compared with beech. Total C concentrations in fresh litter were similar for all deciduous species and showed similar decreases for beech and oak (Table 3). For cherry, C concentrations initially increased and then also decreased. Pine had the highest initial C concentration of all litter (539 mg g 1) and remained fairly unchanged after 0.5 years and decreased for the second sampling but was still higher than for cherry. Initially, oak was the highest in N and P followed by beech, cherry and pine, while C-to-N ratios increased in the same order. In contrast to carbon, N concentrations generally increased during decomposition and concomitantly C-to-N ratios decreased. The biggest increase in N concentration was found for cherry, while smaller changes were observed for pine, oak and beech. The C-to-N ratio for each sampling remained higher for beech litter than for oak, and for pine litter compared with cherry. Phosphorus concentrations distinctly increased for pine and cherry after 0.5 and 2 years, while they only slightly increased for oak but decreased for beech. Table 4 summarizes data for total and percentage extractable condensed tannins and total phenolics in plant litter before and after two periods of decomposition. Owing to the lack of specific standards for each species, the absolute values are not reliable, although the analyses reflect the pattern of changes in concentrations of tannins and phenolics with time (Kraus et al. 2003a). Fresh beech litter was distinctively higher in condensed tannins (CT) compared with oak, while percentage extractable tannins and total phenolics were fairly similar. This is probably due to oak having a higher proportion of hydrolysable tannins (HT) that are detected by the phenolic assay, but not by the proanthocyanidin assay specific for condensed tannins. Cherry litter was distinctively higher in total tannins and phenolics compared with pine, while differences in the extractable tannin portion were small. Tannin concentrations and particularly the extractable fraction decreased very fast for all litters during Table 3 Carbon, N and P concentrations and C/N ratios of fresh and decomposed litter
Beech
Species
0.5-year decomposition Remaining mass (%)
2-year decomposition Remaining mass (%)
Oak
Beech Oak Pine Cherry
85.5 60.5 49.6 31.7
65.4 (10.5) a 25.0 (9.0) b 31.7 (12.1) a 5.4 (3.5) b
Pine
a
(4.0) (5.1) (4.2) (5.6)
a b a b
Standard deviations in parentheses. Means followed by different letters are significantly different (P110 ppm 3· raised for fresh oak litter)
The spectra of fresh litters are shown in Figs. 1a and 2a. Intensity in the alkyl region (0–50 ppm) arises largely from surface waxes and cutin. Long-chain CH2 typically
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Fig. 2 13C CPMAS NMR spectra of fresh (a) and 2-yeardecomposed (b) pine and cherry litter (Insert >110 ppm 5· raised for fresh pine and 4· raised for fresh cherry litter, respectively)
gives a split peak, with maxima at 30 and 33 ppm associated with more mobile and rigid chains, respectively. These are found for all species, although for pine, the 30-ppm peak is reduced to a shoulder of the 33-ppm peak. For pine, the alkyl region is sharp and rather featureless with a maximum at 33 ppm, but the broader profiles for the deciduous litters indicate a greater variety of alkyl structures. Oak and beech have additional distinct peaks at 22 ppm, and cherry at 40 and 48 ppm. The sharp O- and di-O-alkyl peaks at 72 and 105 ppm arise mainly from carbohydrates. There is some variety in spectral features of the O-alkyl region. Sharper features and increased splitting in pine indicate increasing cellulose content and larger crystallites, while the broader peaks in the deciduous litter would be associated with a higher proportion of non-cellulosic polysaccharides, or cellulose with decreasing crystallite dimensions. Carboxyl, amide and ester carbons (including those in acetate, cutin, proteins and hydrolysable tannins) give rise to the peak at 175 ppm. Tannins and lignins are the main contributors in the aromatic and phenolic regions. While the peak positions
in the region from 140–165 ppm are affected by the degree of etherification at C-4, softwoods with a predominance of guaiacyl lignin generally have a peak at 148 ppm with a shoulder at 153 ppm, as in the spectrum of pine. The syringyl lignin of hardwoods has a peak at 153 ppm with a shoulder at 146 ppm; the phenolic region thus reflects the relative proportion of syringyl versus guaiacyl lignin. Lignin also produces the methoxyl signal at 56 ppm in all spectra. For condensed tannins, the phenolic region has a characteristic split peak at 144 and 154 ppm. These characteristic tannin peaks are most distinct for beech. The situation is more complex for some angiosperms like oak, which also have hydrolysable tannins. Tannic acid (mainly a-1,2,3,4,6-pentagalloyl D-glucose) has peaks at 140, 146 and 165 ppm (Kraus et al. 2003a). The relative areas of the initial litters (Table 5) show only small differences, despite the large differences in mass loss. Pine and cherry are slightly higher in O-alkyl C, and lower in aromatic plus phenolic C, while cherry has the highest ratio of alkyl/O-alkyl C. Further qualitative information on C structures is available from the DD spectra, shown in Fig. 3a. The DD spectra retain intensity from carbons without attached hydrogens, as well as from carbons with some mobility in the solid-state, such as CH2 in long chains
183 Table 5 Relative intensities (percentage of total area) of the O-alkyl ratios
Beech Oak Pine Cherry
Initial 2 years Initial 2 years Initial 2 years initial 2 years
13
C CPMAS NMR spectra of fresh and 2-year-decomposed litter; alkyl-to-
Alkyl
Methoxyl
O-alkyl
di-O-alkyl
Aromatic
Phenolic
Carboxyl
Alkyl/O-alkyl
19.7 18.7 18.4 22.3 21.1 22.4 23.0 21.6
5.7 8.1 6.5 7.3 5.6 7.5 6.0 6.8
42.1 39.9 42.3 37.9 45.6 38.6 44.7 37.4
12.1 11.7 12.2 11.1 11.7 10.3 11.8 12.0
9.8 10.7 9.6 10.1 7.9 11.2 8.0 10.4
6.1 6.0 6.1 6.0 4.4 5.9 3.2 6.7
4.5 5.8 5.0 5.4 3.7 4.3 3.2 5.2
0.33 0.31 0.30 0.40 0.34 0.40 0.37 0.38
(the peak at 30 ppm) and OCH3. A characteristic peak of condensed tannins is found at 105 ppm in DD spectra, a region usually free of other peaks. Because intensity is concentrated in the aromatic, phenolic and carboxyl regions, sideband suppression was used to give undistorted peak shapes and positions. The DD spectrum for cherry clearly shows the predominance of tannin versus lignin structures. The phenolic region has two well-resolved peaks at 145 and
Fig. 3 DD-TOSS 13C CPMAS NMR spectra of fresh (a) and 2-year-decomposed (b) litter
155 ppm, and a sharp signal at 105 ppm, whereas the methoxyl signal at 56 ppm is very weak. Compared with the other species, cherry is also notable for the predominance of intensity in the alkyl region, including sharp signals at 17, 30, 38, 40, 42 and 48 ppm, more clearly resolved than in the normal CP spectrum. The pine DD spectrum indicates a mixture of lignin and tannin structures, with peaks at 56, 105, 146 and 154 ppm, as well as peaks for mobile alkyl C at 15, 21 and 30 ppm. Both oak and beech have mobile C, with sharp peaks at 21 and 30 ppm, and methoxyl at 56 ppm. For oak, the phenolic peaks at 145 and 153 ppm may be largely due to lignins (syringyl and guaiacyl) and
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hydrolysable tannins. The latter is consistent with the low intensity at 105 ppm, and the chemical analysis yielding relatively low condensed tannins compared with total phenolics. By contrast, the DD spectrum of beech indicates lignins plus condensed tannins, the main peak of syringyl lignin and the 154-ppm peak of condensed tannin combining to give the higher intensity at 154 ppm (Preston 1999). To summarize, qualitatively, the DD spectra and chemical analysis are consistent with cherry having high condensed tannin and very low lignin, pine with guaiacyl lignin and condensed tannin, oak and beech with syringyl and guaiacyl lignin, but tannins being predominantly hydrolysable for oak and condensed for beech.
Decomposed litters The CP spectra show only small differences in relative intensity after two years decomposition (Table 5) despite mass losses up to 95% (Figs. 1b, 2b). The percentage of O- plus di-O-alkyl C decreases, more for pine and cherry, which had higher initial values than oak and beech. By contrast, the proportion of aromatic plus phenolic C increases for pine and cherry, but hardly changes for oak and beech. Methoxyl and carboxyl C increase slightly in most cases. The ratio of alkyl/O-alkyl C does not show a consistent pattern, increasing for pine and oak, decreasing slightly for beech, and not changing for cherry. The 2-year spectra (Figs. 1b, 2b) mainly show some broadening of peaks, although for all spectra the 30- and 33-ppm signals can be distinguished, as can the decrease of the O- and di-O-alkyl regions relative to other regions. The DD spectra also show only small changes (Fig. 3b). The signal-to-noise ratio is better, despite fewer scans (usually 8,000 compared with 18,000), reflecting the accumulation of non-protonated C. The carboxyl peak at 175 ppm increases, compared with other signals, and the intensity of the sharp lines in the alkyl region decreases. In contrast to the almost complete loss of tannins and phenolics, even within 6 months, all spectra retain a broad signal at 105 ppm. The pattern of change in the phenolic region is variable. The peak shapes and positions are basically unchanged for beech. Cherry retains the split peak characteristic of tannins, but accumulation of lignin is reflected by the stronger methoxyl signal at 56 ppm and the shift from 155 to 153 ppm. The phenolic region becomes typical of lignin for pine (148 ppm, shoulder at 152 ppm) and oak (153 ppm, broad shoulder at 145–148 ppm). These are now similar to the DD phenolic regions shown by Manders (1987) for wood of southern pine (Pinus spp.) and red oak (Quercus spp.). Thus, while there was a general trend for loss of sharp lines of mobile C, and an increase in carboxyl and methoxyl C, there was no consistent pattern for loss or accumulation of tannins versus lignins, and tannin structural components appear
to be retained, even when tannins and phenolics can barely be detected by our chemical methods (Hernes et al. 2001; Lorenz et al. 2000; Preston 1999). Difference spectra Figure 4 shows the difference spectra obtained by subtraction of spectra of initial litter from spectra after 2 years of decomposition. These show mainly structures accumulating, compared with difference spectra of losses shown by Almendros et al. (2000) for nine species. The spectra include some sharp negative-going features, that are more pronounced for cherry and pine than for oak and beech. While not all are clearly discriminated for all species, these peaks are found at 65, 72, 75, 85, 89 and 105 ppm, corresponding to the peak positions of cellulose. The broader positive features are also more clearly developed for cherry and pine, consistent with the larger changes in relative intensities. The increases in the alkyl and carboxyl region may be due to preservation of cutin and waxes, and also to accumulation of protein, as all litters increased in N concentration with decomposition. The peak at 56 ppm with a shoulder at 60 ppm is likely due to increased relative intensity
Fig. 4 Difference spectra obtained by digital subtraction of the fresh from the 2-year spectra 13C CPMAS NMR spectra
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for both methoxyl C, and also to a-C of protein, the intensity of which would be lost in the DD spectrum. For cherry and pine, in the region of about 90–160 ppm, the broad envelope of positive peaks is mainly interrupted by the sharp negative peak at 105 ppm. For cherry, the split phenolic peak at 145 and 155 ppm and low intensity at 130 ppm indicates accumulation of tannin structures, whereas for pine, the phenolic peak at 148 ppm, broader aromatic intensity at 130 ppm, and sharper, more intense peak at 56 ppm are consistent with lignin structures. The confused patterns in the Oand di-O-alkyl regions then reflect a combination of carbohydrate loss, but accumulation of other biopolymers. The 3-carbon lignin side chain occurs in the region, as do C2 and C3 of tannins, and some carbons of cutin. The decomposition study of nine litters by Almendros et al. (2000) involved laboratory composting for a shorter time (168 days), at a higher temperature (28 C), and without the leaching that was important in our field study. However, a key point of similarity is that no single pattern of change in C composition was detected. Early decomposition processes were highly variable by species, and could include, for example, both loss of tannins and their accumulation in the more stable fraction.
Discussion Comparison of litter chemistry Litter quality, the physical and chemical nature of the litter, can largely explain different decomposition rates at a plot scale if climatic variables are reasonably similar (Berg et al. 1993; Fioretto et al. 1998; Preston et al. 2000). Fresh beech litter had a higher C-to-N ratio compared with oak, while pine had a higher C-to-N ratio than cherry. This indicates a comparatively lower quality of beech and pine in terms of decay rate compared with oak and cherry (Enriquez et al. 1993; Pe´rezHarguindeguy et al. 2000). Furthermore, the lower N concentration of beech compared with oak, and those of pine compared with cherry could be related to lower initial decay rates for beech and pine (Berg 2000; Berg et al. 1982). The distinctively higher initial P concentration of cherry compared with pine indicated also a higher mass loss for Prunus serotina litter. For pineneedle decomposition, Staaf and Berg (1982) observed a close correlation between initial P content and mass loss. However, differences between beech and oak litter in P concentration were small. Beech litter was distinctively higher in chemically identifiable tannins compared with oak, and cherry higher than pine indicating lower decomposability of beech and cherry (Kraus et al. 2003b). Concentrations of total phenolics in beech and oak were reasonably similar, but almost twofold higher in cherry than in pine. If the high total phenolics in cherry litter affects
decomposability is unclear, as the Folin-based method provides a broad measure of all readily oxidized compounds (cf. Schofield et al. 1998). Litter quality of fresh beech and oak litter as seen by NMR spectrosopy was reasonably similar. However, beech was slightly higher in alkyl C, and this intensity arises largely from surface waxes and cutin. Cutin is highly resistant to decomposition and is related to physical toughness (Gallardo and Merino 1993; Preston et al. 1997). NMR spectra also indicated higher tannin contents for beech than for oak. Differences in spectra between cherry and pine were obvious. For cherry litter, higher contents of surface waxes and cutin, but lower lignin contents compared with pine, were indicated. Black cherry has a typical herbaceous lignin, and the chemically identifiable lignin content is low (Reh et al. 1990). The initial lignin content is often negatively correlated with the rate of decay (Gholz et al. 2000; Preston et al. 2000). Summarizing the results from the chemical analysis, beech and pine are lower in N and P and higher in C-to-N ratio, so should decompose more slowly. Beech is higher in tannins but about the same in phenolics as oak, so would probably decompose more slowly. However, cherry is higher in tannins and phenolics than pine. Differences in NMR between beech and oak are small, but probably consistent with lower rates of decomposition for beech. Differences between cherry and pine are also actually rather small, but would predict slower decomposition for cherry. The nutrient indices are therefore good predictors of decomposition rates, but the organic parameters are inconsistent. Litter decomposition At the end of this 2-year decomposition study, there was a loss of 34.6–75.0% of litter mass in the study with beech and oak, and a loss of 68.3–94.6% in the study with pine and cherry. However, all litters showed the highest mass loss until the first sampling. After 0.5 years, more than 90% of total tannins were lost, while the percentage of extractable tannins decreased by 70–100%. Total phenolics also disappeared quickly until the first sampling. This rapid tannin loss exceeded previously reported losses in the range of 80% within 1 year for deciduous and coniferous litter (Lorenz et al. 2000). Leaching and immobilization are responsible for the rapid decrease in tannins and phenolics (Hernes et al. 2001; Schofield et al. 1998). The intense leaching and high mass loss during the first half year (December–May) can partly be explained by the high precipitation. Compared with the 30-year averages (Schirmer and Vent-Schmidt 1979), actual precipitation was distinctively higher (249 vs. 348 mm; unpublished data). However, due to tighter packing in the litterbags, mass losses for beech and oak after 0.5 years were lower than for pine and cherry. This was also confirmed by NMR as O-alkyl C losses, including
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soluble carbohydrates, were distinctively lower for beech and oak than for pine and cherry. A strong influence of winter precipitation (October–March) in year 1 of decomposition of ten foliar litters was reported by Trofymow et al. (2002). Factors controlling initial massloss rates have been related to the loss of soluble compounds including soluble carbohydrates, phenolics, and tannins (Berg and Tamm 1991). Beech litter decayed more slowly than oak as had also been reported by Cortez (1998). The slower decomposition was explained partly by a lower initial palatability of beech leaves for earthworms due to high lignin and polyphenol contents (Tian et al. 1995). Higher chemically identifiable acid detergent fibre and lignin contents of beech compared with oak were also reported by Sariyildiz and Anderson (2003). Furthermore, tannins can reduce digestibility and palatability of plants and reduce microbial activity (Lorenz et al. 2000). Therefore, the higher total and extractable tannin concentrations and higher concentrations of phenolics for beech after 0.5 and 2 years can partly explain the lower decomposition rate compared with oak. Further evidence for the faster decomposition of oak is indicated by the comparatively strong decrease in O-alkyl C, associated with carbohydrates. This loss was accompanied by an increase in alkyl-to-O-alkyl ratio indicative of a comparatively high degradation rate of carbohydrates regarding lipid bio-macromolecules (Baldock et al. 1997). Furthermore, N and P concentrations for beech were lower at each sampling and C-to-N ratios higher than for oak, both indicative of a lower decay rate (Berg and Ekbohm 1991; Pe´rez-Harguindeguy et al. 2000; Staaf and Berg 1982). However, in-growth of roots and fungal hyphae into the litterbags might also have contributed to changes in N and P concentrations (Berg and Staaf 1981; Hasegawa and Takeda 1996; Lisanework and Michelsen 1994; O’Connell 1989). The black cherry leaves decayed very fast compared with pine needles. This was in agreement with observations by Kratz (1991) who could not find any cherry litter after 2.5 years, while 20% of the initial pine litter still remained. Rapid decay of black cherry litter was also observed by Adams and Angradi (1996). The fast decomposition of cherry can partly be explained by its low chemically identifiable lignin content and its high content of soluble carbohydrates (Boerner and Rebbeck 1995; Reh et al. 1990). Experiments of Bornebusch (1953) showed that earthworms, notably Lumbricus terrestris, have a higher preference for feeding on black cherry leaves than for feeding on pine needles. However, on our site, earthworms are not very abundant and Lumbricus terrestris is even absent (Ehrmann, personal communication). In contrast, phytophagous insects are impeded while feeding on cherry leaves as they contain the toxic cyanogenic glycoside prunasin (Horsley and Meinwald 1981; Schroeder 1978). Among 14 deciduous species, cherry leaves were most sensitive to atmospheric ozone, indicating low toughness of cherry leaves (Van der Heyden et al. 2001).
However, the big differences in mass loss in our study were not in accordance with changes in litter quality in terms of tannins, phenolics and NMR. Condensed tannins and phenolics decreased very fast for both litters. The short-lived cherry leaves were even comparatively higher in defence chemicals (tannins, phenolics) and leaf toughness (cutin, as indicated by NMR) than the longlived pine needles. In a 3-year study with 36 foliar litters, including deciduous and coniferous, NMR parameters had also a low predictive value for mass loss (Preston et al. 2000). Hence other litter properties, such as concentrations of P, S, Mn and Ca, may have contributed to differences in mass-loss rates in our study (cf. Berg 2000). Similar to the first study on deciduous litter decomposition, N and P content and C-to-N ratio had a higher predictive value for mass loss. Cherry was always higher in N and P and had lower C-to-N ratios compared with pine, indicating a higher decay rate for cherry litter. As with the first study, interpretation of changes in nutrient concentration is hampered by possible nutrient transfer from in-growing roots and fungal hyphae.
Conclusions Carbon-13 CPMAS NMR spectra of four foliar litters showed only minor differences in organic composition. The mass losses in both 2-year decomposition studies could not be related to changes in litter quality as seen by NMR. Oak lost 2.5 times more mass than beech over 2 years, and this was partly explained by the higher initial N and P concentrations and lower C-to-N ratios. Furthermore, differences in leaf palatability and toughness and nutrient contents may also have contributed. In contrast, the six times higher mass loss for cherry compared with pine could hardly be explained by chemical analysis and NMR. Leaching was mainly responsible for the initial losses of mass, tannin, phenolics and other soluble compounds. However in later stages, high N and P concentrations and low C-to-N ratios helped to explain high decay rates. The limitations of both NMR and chemical analysis indicate the need for molecular-level analysis to obtain a more complete understanding of the organic composition of litter and its decay. For our study site, there is clear evidence that the fast decay of black cherry leaf litter plays a major role in the present humus dynamics. There is a clear trend towards biologically more active humus forms with a narrower C-to-N-ratio. This trend implies also an increased availability of N (and P). Since black cherry has a high N demand, which is mainly met by root uptake from the forest floor, this species is crucial for internal N cycling. Perhaps also the high tannin concentration of cherry can help sequester N. In total, all effects appear to result in a distinct prevention of nitrate leaching into groundwater. This is an important issue since the studied conurbation forest, which is subject to a continued high N deposition level, is a major drinking water source. Under the
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present site conditions, black cherry appears to be a major constituent of the forest’s function to ensure an appropriate water quality. An abrupt removal of this species from the understorey by applying drastic methods (e.g. mechanical control, including tillage) could have detrimental effects on nutrient leaching: the internal nutrient cycle would be interrupted, and extra mineralization would be likely to occur. The slow displacement of black cherry by the natural species, beech and oak, might therefore be more appropriate. From our experimental studies, however, we are uncertain as to whether the understorey of the two species favored by silviculture is as efficient for N retention as black cherry. Acknowledgements We thank the Mannheim Municipal Water Operations (MVV) for funding the experimental work. In particular, Dr. Ries (water management branch) and the staff of the Ka¨fertal water plant gave valuable logistical and technical support. The Baden-Wu¨rttemberg Forestry Administration (Weinheim District) helped in site selection. The technicians in the Tharandt soil laboratory, B. Kockisch, R. Ru¨ger and M. Unger, carried out the chemical analyses with great diligence. We also thank the International Bureau of the BMBF (German Ministry of Science and Higher Education, Bonn) for funding travel to Canada within the cooperation program between Canada and Germany (WTZproject CAN 98/033).
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