Forest Ecology and Management 133 (2000) 13±22
Litter decomposition and organic matter turnover in northern forest soils BjoÈrn Berg* È K, Postfach 101251, Univ. Bayreuth, Dr. Hans Frisch Strasse 1-3, Lehrstuhl fur BodenoÈkologie, BITO DE-95 448 Bayreuth, Germany Accepted 6 October 1999
Abstract The decomposition rate of fresh plant litter may decrease from ca. 0.1% per day in fresh litter to 0.00001 per day or lower in more completely decomposed material. This is due to changes in its organic-matter quality as the recalcitrant chemical components become enriched in the material. The decrease in decomposability (substrate quality) is complex, involving both direct chemical changes in the substrate itself and the succession in micro-organisms able to compete for the substrate with a given chemical composition. The concept `substrate quality' varies among litter species, though. In fresh litter, there may be a lack of macronutrients, such as N, P, and S thus limiting the decomposition rates of, for example, the celluloses, and the rates may be positively related to, for example, the concentration of N. With the disappearance of celluloses, the concentration of the more recalcitrant compound, lignin, increases and the effects of N concentration on decomposition rates change completely. In partly decomposed litter the degradation rate of lignin determines the decomposition rate of the whole piece of litter, which now in reality is turning into soil organic matter (SOM). At this stage high N concentrations will have a rate-retarding effect on lignin degradation and thus on the litter. It appears that this total retarding effect of N may be ascribed to two different mechanisms. First, low-molecular N reacts with lignin remains creating more recalcitrant aromatic compounds, and, further, low-molecular N may repress the synthesis of lignin-degrading enzymes in white-rot fungi. The retardation of the decomposition rate may be so strong that the decomposition of the litter can be estimated to reach a limit value for total mass loss. At such a stage the litter would be close to more stabilized SOM. The limit values estimated to date range from about 45 to 100% decomposition indicating that between 0 and 55% of the litter mass should either stabilize or decompose extremely slowly. We found that N concentration had an overall effect on this limit value in no less than 130 cases investigated, meaning that the higher the N concentration in the fresh litter (the lower the C/N ratio) the more organic matter was left. The relationship could be described by a highly signi®cant and negative linear relation. Other nutrients were also correlated to the limit value. Thus, Mn and Ca had a generally opposite effect to N, meaning that high concentrations of these nutrients were correlated to further decomposition in all studies investigated. The `limit-value' concept may mean that at higher initial N concentrations, the stage with either stabilized SOM or a very low decomposition rate was reached earlier, i.e. at a lower mass loss. Such an effect would mean that in stands with N-rich litter there may be a faster humus accumulation. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Litter; Soil organic matter
* Tel.: 49-708-212424; 49-921-555799. E-mail address:
[email protected] (B. Berg)
0378-1127/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 9 9 ) 0 0 2 9 4 - 7
14
B. Berg / Forest Ecology and Management 133 (2000) 13±22
1. Introduction The accumulation of soil organic matter (SOM) is a slow process that often spans generations of scientists, thereby causing continuity problems in following the buildup as well as the mechanisms controlling it. Still, a long-term buildup of SOM appears to take place. Thus, Wardle et al. (1997) found a thick mor humus layer that had accumulated for 2900 years under growing trees. Such an SOM buildup is based on remains from decomposing plant litter. By tradition there appears to be a general opinion that climate rules decomposition on a regional scale whereas litter chemical composition dominates the process on a local scale. It appears, though, that the picture may be more complicated than that. Meentemeyer (1978) and later Berg et al. (1993b) showed a large-scale effect by climate on decomposition rate of fresh plant litter. However, such an effect is not general. In contrast, Berg et al. (1998) using the same transect as Berg et al. (1993a) showed that for newly shed Norway spruce litter there was no climate effect. Later decomposition stages of plant litter have been studied less thoroughly than earlier ones, and they clearly deserve further attention. Several studies have reported declining rates with decomposition level (e.g., Fogel and Cromack, 1977; Berg and Lundmark, 1987). Johansson et al. (1995) even found that in a long climatic transect the substrate quality i.e., high lignin concentrations, dominated over the climate effect. For very late stages, Lousier and Parkinson (1976) and later Couteaux et al. (1998) estimated extremely low decomposition rates of the magnitude 10ÿ5% per day. Using another approach, Howard and Howard (1974) described decomposition rates that approached zero, which was con®rmed by Berg and Ekbohm (1991), Berg et al. (1996b). In such cases the accumulated mass loss approaches a ®nal limit value for decomposition which can be described by an asymptotic function. The decomposition in these systems was mainly microbial and with low levels of soil animals. Berg et al. (1996b) and Berg and Johansson (2000) compared limit values for 106 sets of decomposing foliar litter from natural forest systems. Using litters representing a wide range in chemical composition they found a highly signi®cant negative relation between limit values and initial N concentrations in
litter. The level of the estimated limit values have also been related to initial concentrations of other nutrients, such as Mn (Berg et al., 1996b) and lignin (Berg and Johansson, 2000). This approach is not contradictory to that used by Lousier and Parkinson (1976) with a very low decomposition rate in the late stages. However, the approach used by Berg et al. (1996b) makes it possible to quantify the remaining, recalcitrant mass in the very late stages and allows a further evaluation. Thus, if different litter species differ in limit values, i.e. in terms of the proportion of their mass contributed to pools of stable organic matter, then given a constant rate of litterfall, the buildup of soil organic matter should vary depending on the chemical composition of the falling litter, both within a species and between species. In fact, that long-term humus buildup and storage are possible was shown by Wardle et al. (1997) when they determined such a buildup to have taken place for about 2900 years. The aim of this paper was to organize existing knowledge into a possible structure and create a system of in¯uencing factors on litter and SOM decomposition. Further, the intention is to relate the in¯uence of the chemical composition of foliar litter from different tree species to the storage rate of SOM. 2. Discussion 2.1. Model for litter decomposition and chemical changes during decomposition Fresh litter is very different from older, partly decomposed litter from a chemical point of view, thus in¯uencing the rate-regulating factors and the microbial community. Based on their studies on Scots pine litter, Berg and Staaf (1980) set up a model dividing the decomposition into two phases, with an early stage in which climate as well as concentrations of the major nutrients and water solubles had a clear in¯uence on decomposition rate. In a later phase the decomposition of lignin dominated over the in¯uence of nutrients and thus ruled the decomposition of litter (Fig. 1A). Simultaneously the rate decreased and the accumulated mass loss even may approach a limit value (Fig. 1B).
B. Berg / Forest Ecology and Management 133 (2000) 13±22
15
but also over several species (Berg and Ekbohm, 1991). Also, initial concentrations of soluble substances have been related to initial mass-loss rates (Berg and Tamm, 1991). Although the rate-enhancing effect of raised nutrient levels on the decomposition of newly shed litter may be a common phenomenon it is not a general one. Thus, Berg and Tamm (1991) found for Norway spruce needle litter that there was no relationship between initial concentrations of nutrients and mass-loss rates. One possible explanation may be that the needles stay attached to the branches and start decomposing before they fall, thus being in a late stage already when shed. Still, other explanations could not be excluded.
Fig. 1. A. Model for chemical changes and rate-regulating factors during decomposition. Modified from Berg and Matzner (1997). B. Asymptotic model for estimating limit values for plant litter decomposition. Limit value indicated by the dashed line. Redrawn from Berg and Ekbohm (1991).
2.2. Decomposition in the early stages 2.2.1. Substrate quality In the early phase, concentrations of water-soluble substances decrease quickly (in a few months) before reaching relatively similar and stable levels (Berg et al., 1987). Also, free unshielded holocellulose is degraded in this phase whereas the recalcitrant lignin either does not decompose or only to a low extent. Thus, its concentration starts to increase due to the decomposition of other main compounds. Also the concentrations of some nutrients such as N, P and S, start to increase (Staaf and Berg, 1982). In this early phase, the mass-loss rate may be related to total concentrations of the major nutrients, such as N, P and S, which often are limiting for decomposition rates not only within a species (Berg and Staaf, 1980)
2.2.2. Climate influence For newly shed litter it appears that climate may in¯uence litter mass-loss rate (Fig. 2). For needle litter of Scots pine, it has been possible to demonstrate the in¯uence of climate on decomposition rate, both as the annual variation at one site (Jansson and Berg, 1985) and the range in climate within a 2000 km-long climatic transect (Berg et al., 1993b, Fig. 2). Such effects of climate could thus be recorded for local and uni®ed pine needle litter in pine forests with their relatively open canopy covers. The early-stage decomposition rates (measured over the 1st year) ranged from about 10.9% per year close to the Arctic Circle in Scandinavia to about 43.7% year in northern Germany. The dominant rate-regulating
Fig. 2. Linear relationships between annual actual evapotranspiration (AET) and first-year mass loss (from Berg et al., 1993b).
16
B. Berg / Forest Ecology and Management 133 (2000) 13±22
factor was the climate, as indexed by annual actual evapotranspiration (AET), and none of the substratequality factors was signi®cant. On the other hand, in a corresponding transect of Norway spruce forests no effect of climate (as indexed by AET) was seen (Berg et al., 2000), the litter being local spruce needle litter. This lack of climate in¯uence may at present only be subject to speculation. 2.3. Decomposition in late stages 2.3.1. Lignin concentration and litter decomposition rates Concentrations of the recalcitrant sulfuric acid lignin fraction increased as decomposition proceeded, reaching relatively steady levels in the range of 45±51% (Berg et al., 1984). These increases showed partially linear relationships to accumulated mass loss (Berg et al., 1984, 1997). Also concentrations of N and P increased linearly with accumulated mass loss (Staaf and Berg, 1982). As decomposition proceeds the litter becomes enriched in, among other components lignin and N (Berg and Staaf, 1980). Earlier work has shown that as lignin concentrations increase during litter decomposition the decomposition rates are suppressed (e.g., Fogel and Cromack, 1977; McClaugherty and Berg, 1987). The decomposition rate of remaining litter would thus be ruled by lignin degradation rate as the cellulose in the remaining parts would be shielded by lignin. The suppressing effect of lignin on litter mass-loss rates can be described as a linear relationship (e.g., Fogel and Cromack, 1977; Berg and Lundmark, 1987) in the later decomposition stages, which, for pine litter, may start already at ca. 20±30% mass loss (Fig. 3A). For these later stages Berg et al. (1993a) observed that the slope and intercept of this negative relationship varied among sites with different climates. The lowest effect of lignin concentration on mass-loss rates was found near the Arctic Circle (where long-term average AET was about 385± 390 mm) whereas in Northern Germany and on the continent the rate-regulating effect of lignin was higher (Fig. 3B). The steepest slopes were thus obtained for the southern sites which were warmer and wetter (with AET values for site 8 being 509 mm and for site 13, 560 mm) and thus, had initially higher mass-loss rates than the more northern sites (Fig. 3B).
Fig. 3. Linear relationships between lignin concentration in decomposing Scots pine needle litter and annual litter mass loss. A. Available data from one site (JaÈdraaÊs) (recalculated from McClaugherty and Berg, 1987). B. Available data from five climatically different sites with the AET values 385, 387, 472, 509 and 560 mm for sites 2, 3, 6:51, 8 and 13, respectively (from Berg et al., 1993a).
For the northern sites, the slopes were shallow and we may see that lignin concentration had very little effect. Thus, whereas the slope for site No. 13 (Fig. 3B) was ÿ0.250 mg%ÿ1, the slopes were ÿ0.022 and ÿ0.018 mg%ÿ1 close to the Arctic Circle. The slopes for the sites in south (site No. 8) and central Sweden (site No. 6: 51) were in between (Fig. 3B). In a development of this work, Johansson et al. (1995) compared slopes for the signi®cant relationships between lignin concentration and annual mass loss for 11 sites over the full length of the climatic transect. The effect of lignin concentration on litter mass-loss rate thus varied with site climate and this relative effect was negatively related with AET (Fig. 4). Johansson et al. (1995) even found a highly
B. Berg / Forest Ecology and Management 133 (2000) 13±22
17
Fig. 4. Slopes for the relationships of annual litter mass loss plotted vs. the climate index actual evapotranspiration (AET) (cf. Fig. 3B) (from Johansson et al., 1995).
signi®cant relationship between slope and AET (Fig. 4, R2 0.559). 2.3.2. Nitrogen concentration is critical for lignin degradation During late stages of decomposition there was a clear negative relationship between N concentration and lignin mass-loss rate as well as between N concentration and litter mass-loss rate. The lignin decomposition rate was lowest for N-rich litters and highest for N-poor ones (Berg et al., 1982). Also, Berg and Ekbohm (1991) found a clearly signi®cant and negative relationship between N concentration and lignin decomposition which was in common for seven types of litter. They ®tted a highly signi®cant linear model including the N concentration of the litters (R2 0.677). The empirical relationship of N as a rate-suppressing factor could be supported by causal relationships based on two phenomena. These also help to explain why mass-loss rates of the sulfuric acid lignin fraction differed among litters. Keyser et al. (1978) found that low-molecular N compounds repressed the formation of ligno-lytic enzymes in one species of a white-rot fungus. There now appear to be several species which have this kind of repression (Eriksson et al., 1990; P. Ander, pers. comm.). As a further rate-regulating phenomenon, products of lignin degradation may react with ammonia or amino acids to form recalcitrant complexes (NoÈmmik and Vahtras, 1982). Results of laboratory experiments indicated that the concentration of ammonium/ammonia could be rate-limiting for this kind of reaction to proceed (Axelsson and Berg, 1988).
Fig. 5. Comparison between N concentration in humus (F and H layers) and CO2 release rate from the samples incubated under standard conditions (redrawn from a review by Berg and Matzner, 1997).
Combining the above information may give us support to why the lignin of the more N-rich litter had lower mass-loss rates. It is reasonable to assume that either one or both of these mechanisms may contribute to decrease the decomposition rate of sulfuric acid lignin. Also, in partly decomposed litter this compound exists either as native or moderately modi®ed lignin. At least within a certain range of litter mass loss, there does not appear to be any extensive synthesis of entirely new products. Thus, Norden and Berg (1990) did not ®nd any new peaks in the aromatic resonance region when applying high resolution 13C NMR to pine needle litter samples in decomposition stages from 0 to 70% accumulated mass loss. The observation of the repressing effect of N has not been limited to mass-loss measurements. Also, raised N concentrations in humus both as ammonium and as total N, suppress CO2 formation from humus (review by Berg and Matzner, 1997) (Fig. 5). 2.4. The very late stages and the concept `limit value' 2.4.1. General comments When Howard and Howard (1974) and Berg and Ekbohm (1991) described that litter decomposition
18
B. Berg / Forest Ecology and Management 133 (2000) 13±22
appeared to come to a halt they estimated limit values (Fig. 1B) that were signi®cantly different among litter species. Their work was based on the assumption that the sum of decomposition processes resulting in litter mass-loss should continue to slow down without violent breaks in that pattern.
Table 1 Correlations between limit values and initial concentrations in litter of N, P, S, K, Mg, Mn, Ca and lignin, respectivelya
2.4.2. Litter chemical composition and limit values Berg and Johansson (2000) collected from the literature in all 106 limit values for foliar litter decomposing in natural systems. When regressing these limit values against concentrations of nutrients and of lignin they found that N concentration gave a highly signi®cant and negative relationship (R2 0.323, n 106, p < 0.001) (Fig. 6A, Table 1). The possible causes for the relationships between limit values and N were discussed above. The fact that in this large data set the relationship to N concentration was
Nutrient
r
R2
n
p<
Natural systems N Mn
ÿ0.568 0.519
0.323 0.269
106 83
0.001 0.001
All deciduous litter Mn Ca N
0.618 0.675 ÿ0.438
0.382 0.456 0.192
13 18 30
0.05 0.01 0.05
All coniferous litter N Mn
ÿ0.660 0.513
0.436 0.263
86 74
0.001 0.001
Scots pine litter alone N Mn
ÿ0.683 0.485
0.466 0.235
42 35
0.001 0.01
Norway spruce needle litter Lignin ÿ0.742 Ca 0.636
0.551 0.404
11 11
0.01 0.05
a With data from all sites pooled the extent of the chemical analyses determined the amount of data in the analysis of each nutrient (different n values). From Berg and Johansson (2000).
Fig. 6. Linear relationship between limit values for decomposition and initial concentrations of nutrients in foliar litter (from Berg and Johansson, 2000). A. Available data from natural forest systems vs. N concentration. B. Available data from Norway spruce forests plotted vs. litter Ca concentration.
signi®cant indicates a general effect of N over a good number of species in the types of ecosystems studied, i.e., deciduous and coniferous ecosystems in boreal and temperate forests. The low R2 value may depend on the fact that in this data set several factors potentially in¯uencing the limit value increased the variation. Thus, for each species, the average value of the limit value was estimated and compared to the average N concentration (Fig. 7, Table 2) and the relationship improved (R2 0.761, n 8, p < 0.01). Also, litter Mn concentrations gave a highly signi®cant but positive relationship (R2 0.269, n 83, Table 1). Manganese is essential for the activity of Mn peroxidase, a lignin-degrading enzyme and enhancing its production (Perez and Jeffries, 1992). It is also involved in the regulation of other lignolytic enzymes, including laccase (Archibald and Roy, 1992) and lignin peroxidase (Perez and Jeffries, 1992). Although the observed effects for selected groups of litters were largely similar to those observed by Berg et al. (1996b), it was possible to carry the analysis further and the litter types could be subdivided into
B. Berg / Forest Ecology and Management 133 (2000) 13±22
19
signi®cant (R2 0.191, p < 0.05) but weaker than that for Mn and Ca concentrations. There was a good set of data for coniferous litters and the group as such gave a highly signi®cant relationship between limit values and litter N concentrations (R2 0.436, n 86, p < 0.001) (Table 1) as did Mn (R2 0.263, n 74). Berg and Johansson (2000) found enough studies using Scots pine to allow a special investigation of the factors regulating the limit value for that speci®c litter species. They found a highly signi®cant and negative relationship between N concentrations and limit values (R2 0.466, n 42, p < 0.001). A positive relationship was found for Mn (Table 1). For the group of Norway spruce needles, a highly signi®cant and negative relationship was found between limit values and the concentration of lignin in litter (R2 0.551, n 11, p < 0.01) (Table 1). Also, a relationship was seen to Ca concentration. However, there was no relationship to N concentration. At least three factors could contribute, alone or together, to explain the limit-value phenomenon; (i) variations in total concentrations of nutrients may result in varying concentrations of available nutrients that would limit the growth or activity of microbial decomposers, thereby limiting litter decomposition for reasons such as those discussed above; (ii) certain of the microorganisms required in a succession to complete the decomposition process may not be present in a given environment; and/or (iii) for one reason or another, populations of soil animals participating in
Fig. 7. The relationship between mean limit values and N concentration for eight different foliar litter types (from Berg and Johansson, 2000). Average values were calculated for litter types for which there was at least four limit values estimated.
groups. Thus, for deciduous litter as a separate group the limit values were best related to litter concentrations of Mn and Ca. Manganese was signi®cant at the p < 0.05 level (R2 0.382, n 13, Table 1) and Ca was positively related (R2 0.456, n 18, p < 0.01). When using all data (Table 1), no effect of Ca could be discerned, but Ca was a signi®cant factor for deciduous litter as a group. Calcium has been found to support the growth of a white-rot fungal species (Marasmius) (Lindeberg, 1944), although the effect was pH dependent in his experiments. For this group of litters the relationship to N was statistically
Table 2 Mean values for limit values for decomposition and N conc. for eight litter types (from Berg and Johansson (2000) (cf. Fig. 7) Litter type
Scots pine (brown needles) Scots pine (green needles) Lodgepole pine Norway spruce Silver fir Common beech Pyrenean oak White birch
Average values for N conc.
Average limit value
N
SD
SE
Limit value
SD
SE
n
4.19 12.18 4.0 5.44 12.85 11.9 12.2 9.55
0.57 2.57 0.51 1.42 0.66 4.85 3.60 2.74
0.19 0.91 0.19 0.37 0.33 2.17 1.80 1.37
81.3 67.2 94.91 74.07 51.5 59.12 60.3 77.7
6.11 9.55 5.14 13.9 2.52 8.51 7.9 15.6
1.21 3.38 1.94 3.59 1.36 3.81 3.95 7.8
23 8 7 15 4 5 4 4
20
B. Berg / Forest Ecology and Management 133 (2000) 13±22
generally higher N concentrations. The leaves of common beech formed an extreme group with very high concentrations of both N and lignin based on data collected over western Europe. Berg and Johansson (2000) concluded that the distribution pattern for data collected over a larger region were similar to those obtained for a few nearby stands. 2.6. Some observed differences among tree species Fig. 8. Concentrations of lignin and N in newly shed foliar litter of Scots pine (&), lodgepole pine (&), Norway spruce (*), white birch (~) and common beech (*). All available data. (Redrawn from Berg and Johansson, 2000).
the mechanical breakdown of litter have reached too low a level. 2.5. How much do some critical chemical components vary between litter types within a region? Berg and Johansson (2000) showed that different litter types may be grouped according to chemical composition (Fig. 8). The two components, N and lignin have an overall role in the retardation of litter decomposition (Berg and Matzner, 1997). When plotting available data on concentrations of N and lignin for foliar litter, Berg and Johansson (2000) found that the litter types actually formed distinct groups. It may be emphasized that the litter species formed these groups in spite of the fact that the sampling was made in large geographical regions, e.g. the magnitude of Scandinavia. Thus, Scots pine needle litter formed a homogeneous group that did not overlap with the lodgepole pine or Norway spruce groups (Fig. 8). In this comparison, Scots pine needle litter was characterized as having simultaneously low concentrations of both N and lignin whereas lodgepole pine litter formed another homogeneous group, with low N and high lignin concentrations. Norway spruce needles formed a group that had higher N concentrations than those of the two pine species and lignin concentrations that were in between. The birch leaves had lignin concentrations similar to those of the spruce needles and
If the hypothesis presented above holds, it would be possible to distinguish differences in humus buildup among tree species, provided that suitable test systems are found. Although limit values for litter mass loss have been estimated for a variety of litters by using asymptotic functions, we cannot conclude that such limit values indicate that the remaining organic matter is completely undegradable. Instead, the residual organic matter could very well consist of a moderately stabilized fraction that decomposes very slowly or a fraction that just does not decompose in a given environment. However, this would not mean that the discovery of an apparent ®nal mass-loss value should be considered trivial, especially if the limit value could be related to climate and litter properties, e.g., lignin concentration, nutrient status or other environmental factors. In fact, when Berg et al. (1996a) compared C storage in the humus layer in paired stands of Norway spruce and Scots pine, the humus buildup could be related to different limit values for the two species. Further, Berg et al. (1995) were able to reconstruct and validate the build-up of a humus layer in a Scots pine forest. In a review, Cole et al. (1995) compared the organic matter build-up under red alder and Douglas ®r and found a much higher store of organic matter under the former than could be explained by litterfall. Although the conclusive experiment or observation is lacking but the existing data support the hypothesis of a mechanism to estimate organic matter buildup. Acknowledgements Financial support for this work was provided by German Ministry for Education, Science, Research and Technology (BMBF, Grant No BEO-51-
B. Berg / Forest Ecology and Management 133 (2000) 13±22
033947617) to Dr. BjoÈrn Berg, while working as a È K, University of Bayreuth. guest scientist at BITO
References Archibald, F., Roy, B., 1992. Appl. . Appl. Environ. Microbiol. 58, 1496±1499. Axelsson, G., Berg, B., 1988. Fixation of ammonia (15N) to Scots pine needle litter in different stages of decomposition. Scand. J. For. Res. 3, 273±280. Berg, B., Ekbohm, G., 1991. Litter mass-loss rates and decomposition patterns in some needle and leaf litter types. Long-term decomposition in a Scots pine forest VII. Can. J. Bot. 69, 1449± 1456. Berg, B., Johansson, M.-B., 2000. A maximum limit for foliar litter decomposition Ð a synthesis of data from forest systems. Environ. Rev. XX, XXX-XXX, submitted for publication. Berg, B., Lundmark, J.E., 1987. Decomposition of needle litter in lodgepole pine and Scots pine monocultures Ð a comparison. Scand. J. For. Res. 2, 3±12. Berg, B., Matzner, E., 1997. Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ. Rev. 5, 1±25. Berg, B., Staaf, H., 1980. Decomposition rate and chemical changes of Scots pine needle litter. II. Influence of chemical composition. In: Persson, T. (Ed.), Structure and Function of Northern Coniferous Forests Ð An Ecosystem Study. Ecol. Bull. (Stockholm) vol. 32, pp. 373±390. Berg, B., Tamm, C.O., 1991. Decomposition and nutrient dynamics of litter in long-term optimum nutrition experiments. I. Organic matter decomposition in Norway spruce (Picea abies) needle litter. Scand. J. For. Res. 6, 305±321. Berg, B., Johansson, M.B., Lundmark, J.E., 1996a. Uppbyggnad avorganiskt material i skogsmark Ð har goÈdsling och traÈdslagsval en inverkan? In: Berg, B. (Ed), Markdagen, 1996. Report from Departments of Forest Ecol. and Forest Soils. Swed. Univ. Agric. Sci. Report 72, pp. 33±44. (In Swedish). Berg, B., Staaf, H., Wessen, B., 1987. Decomposition and nutrient release in needle litter from nitrogen-fertilized Scots pine (Pinus silvestris) stands. Scand. J. For. Res. 2, 399±415. Berg, B., McClaugherty, C., Johansson, M.-B., 1997. Chemical changes in decomposing plant litter can be systemized with respect to the litter's initial chemical composition. Reports from the Departments of Forest Ecol. and Forest Soils, Swed. Univ. Agric. Sci. Report 74, 85 pp. Berg, B., Meentemeyer, V., Johansson, M.-B., 2000. Litter decomposition in a climatic transect of Norway spruce forests Ð climate and lignin control of mass-loss rates. Can. J. For. Res. XX, XXX±XXX, submitted for publication. Berg, B., Ekbohm, G., McClaugherty, C., 1984. Lignin and holocellulose relations during long-term decomposition of some forest litters. Long-term decomposition in a Scots pine forest IV. Can. J. Bot. 62, 2540±2550.
21
Berg, B., Wessen, B., Ekbohm, G., 1982. Nitrogen level and lignin decomposition in Scots pine needle litter. Oikos 38, 291±296. Berg, B., McClaugherty, C., Johansson, M., 1993a. Litter mass-loss rates in late stages of decomposition at some climatically and nutritionally different pine sites. Long-term decomposition in a Scots pine forest VIII. Can. J. Bot. 71, 680±692. Berg, B., McClaugherty, C., Virzo De Santo, A., Johansson, M.-B., Ekbohm, G., 1995. Decomposition of forest litter and soil organic matter Ð a mechanism for soil organic matter buildup? Scand. J. For. Res. 10, 108±119. Berg, B., Ekbohm, G., Johansson, M.-B., McClaugherty, C., Rutigli- ano, F., Virzo De Santo, A., 1996b. Maximum decomposition limits of forest litter types Ð a synthesis. Can. J. Bot. 74, 659±672. Berg, B., Berg, M., Bottner, P., Box, E., Breymeyer, A., Calvo de Anta, R., Couteaux, M., Gallardo, A., Escudero, A., Kratz, W., Madeira, M., MaÈlkoÈnen, E., Meentemeyer, V., MunÄoz, F., Piussi, P., Remacle, J., Virzo De Santo, A., 1993b. Litter mass loss in pine forests of Europe and Eastern United States as compared to actual evapotranspiration on a European scale. Biogeochem. 20, 127±153. Cole, D.W., Compton, J.E., Edmonds, R.L., Homann, P.S., Van Mie-groet, H., 1995. Comparison of Carbon Accumulation in Douglas Fir and Red Alder Forests. In: McFee, W.W., Kelly, J.M. (Eds.), Carbon forms and functions in Forest Soils. Soil Science Society of America Inc. Madison, WI, USA, pp. 527± 546. Couteaux, M.-M., McTiernan, K., Berg, B., Szuberla, D., Dardennes, P., 1998. Chemical composition and carbon mineralisation potential of Scots pine needles at different stages of decomposition. Soil Biol. Biochem. 30, 583±595. Eriksson, K.-E., Blanchette, R.-A., Ander, P., 1990. Microbial and enzymatic degradation of wood and wood components. Springer Series in Wood Science. Springer, Berlin. Fogel, R., Cromack, K., 1977. Effect of habitat and substrate quality on Douglas fir litter decomposition in western Oregon. Can. J. Bot. 55, 1632±1640. Howard, P.J.A., Howard, D.M., 1974. Microbial decomposition of tree and shrub leaf litter. 1. Weight loss and chemical composition of decomposing litter. Oikos 25, 311±352. Jansson, P.E., Berg, B., 1985. Temporal variation of litter decomposition in relation to simultated soil climate. Longterm decomposition in a Scots pine forest V. Can. J. Bot. 63, 1008±1016. Johansson, M.-B., Berg, B., Meentemeyer, V., 1995. Litter massloss rates in late stages of decomposition in a climatic transect of pine forests. Long-term decomposition in a Scots pine forest. IX. Can. J. Bot. 73, 1509±1521. Keyser, P., Kirk, T.K., Zeikus, I.G., 1978. Ligninolytic enzyme of Phanerochaete chrysosporium: synthesized in the absence of lig nin in response to nitrogen starvation. J. Bacteriol. 135, 790±797. Lindeberg, G., 1944. Ueber die Physiologie ligninabbauender Boden hymenomyzeten. Symb. Bot. Upsal. VIII(2),183 pp. Lousier, J.D., Parkinson, D., 1976. Litter decomposition in a cool temperate deciduous forest. Can. J. Bot. 54, 419±436.
22
B. Berg / Forest Ecology and Management 133 (2000) 13±22
Meentemeyer, V., 1978. Macroclimate and lignin control of litter decomposition rates. Ecology 59, 465±472. McClaugherty, C., Berg, B., 1987. Cellulose, lignin and nitrogen levels as rate regulating factors in late stages of forest litter decomposition. Pedobiologia 30, 101±112. Norden, B., Berg, B., 1990. A non-destructive method (solid state 13 C-NMR) determining organic±chemical components in decomposing litter. Soil Biol. Biochem. 22, 271±275. NoÈmmik, H., Vahtras, K., 1982. Retention and fixation of ammonium and ammonia in soils. In: Stevenson, F.J. (Ed.),. Nitrogen in agricultural soils. Agronomy monographs, No. 22. Agronomy Society of America, Madison, WI, pp. 123±171.
Perez, J., Jeffries, T.W., 1992. Roles of manganese and organic acid chelators in regulating lignin degradation and iosynthesis of peroxidases by Phanerochate chrysosporium. Appl. Environ. Microbiol. 58, 2402±2409. Staaf, H., Berg, B., 1982. Accumulation and release of plant nutrients in decomposing Scots pine needle litter. Long-term decomposition in a Scots pine forest II. Can. J. Bot. 60, 1561± 1568. Wardle, D.A., Zachrisson, O., HoÈrnberg, G., Gallet, C., 1997. The influence of Island Area on ecosystem properties. Science 227, 1296±1299.
![[Squadron-Signal] - [In Action 012] - B-17](https://docer.tips/img/300x300/squadron-signal-in-action-012-b-17_5a5c4cded64ab2c995e6f13f.jpg)
