Variation in Mass-Loss Rate of Foliar Litter in Relation to Climate and Litter Quality in Eurasian Forests : Differences among Functional Groups of Litter

With a data set of litter decomposition collected by means of literature survey, our objectives are 1) to determine the differences in the variation in the first-year mass loss (%) of leaf litter with regard to climate and litter quality among different functional groups of tree species in Eurasian forests, and 2) to determine the difference in effect of mean annual temperature (°C), annual precipitation (dm), as well as concentration of nitrogen (%), and lignin (%) on first-year mass loss over a wide range in climate and litter quality. The main results are as follows. 1) The significant differences between litter types in the relationships between firstyear mass loss and climatic factors plus litter quality revealed clearly different decomposition patterns over the continent. Thus, differences were found between coniferous and broadleaf litter, between deciduous broadleaf and evergreen broadleaf as well as between genera and even within a genus, viz. between deciduous and evergreen Quercus. 2) With a change in a relative unit of climate and litter quality variables, there were clear differences in effects of mean annual temperature, annual precipitation, and nitrogen on first-year mass loss for different functional groups of trees. 3) We identified some broadleaf litter species that decomposed to 100% in one year and thus did not contribute to carbon sequestration in a humus layer. Thus, the variation in pattern of foliar litter decomposition with climate and litter quality across functional groups in Eurasian forests showed different decomposition strategies for litter of different groups and genera.


Introduction
Litter decomposition is an essential process in ecosystems, concerning the emission and storage of carbon (C), nutrient release, as well as formation of humic substances in the soil (Swift et al. 1979, Pastor and Post 1986, Coûteaux et al. 1995, Berg 2000, Parton et al. 2007).As seen in some studies, global forest litter production has been estimated to be as high as 29 × 10 15 g yr -1 (Lonsdale 1988).Foliar litter occupies a major fraction of the litter in forest ecosystems (Matthews 1997) and may be totally decomposed within a year in subtropical and tropical areas (Meentemeyer 1984).It is thus of importance to investigate the pattern of forest litter decomposition and influencing factors for a deeper understanding of global carbon dynamics.
The decay rate of newly shed litter is controlled by several major factors, which may be dependent on the scales across which an investigation is conducted.Such factors may be litter quality (e.g.Melillo and Aber 1982), site conditions including microbial community (e.g.Vitousek et al. 1994, Liu et al. 2001) or plant type (e.g.Cornelisen 1996, Hobbie 1996).At a regional to global scale the process can be related mainly to climate and litter quality (Meentemeyer 1978, Aerts 1997, Moorhead et al. 1999, Liski et al. 2003, Zhang et al. 2008).
In previous studies, the pattern of leaf litter mass loss was demonstrated by combining litter species (e.g.Meentemeyer 1984) or by using just one genus (e.g.Liski et al. 2003), but few comparisons have been made about differences in mass-loss pattern among groups of foliar litter species along a broad climate gradient.We have as a working hypothesis that there are differences between functional groups in-mass loss pattern in relation to climatic and substrate-quality factors.
The objectives of this study were, (i) to determine the overall patterns of first-year mass loss (FML) of foliar litter versus climatic and litterquality variables in Eurasian forests; (ii) to determine the difference in the relationships of FML with climate and litter quality among different genera and functional groups; (iii) to determine relative effects of mean annual temperature (MAT, Temperature, °C), annual precipitation (APT, Precipitation, dm) as well as of nitrogen (N, %) and lignin on FML at a continental scale.
The Eurasian continent comprises a variety of climatic conditions, and a broad diversity of tree species, which provides a way to demonstrate the relationships between litter mass loss, climatic factors and litter quality at a continental scale.Eurasian forests currently cover more than 1.6 × 10 9 ha, making up 41% of the total global forested area (FAO 2001), and CO 2 emission and soil storage of C from litter decomposition is thus an important component in the global carbon fluxes.

Data Collection
The data used in this study were collected by survey of literature, and a data set of 295 FML values of foliar litter was compiled including data on concentration of N and lignin (Appendix A).Not all litter-quality variables were always available.We thus had 124 sets with values for concentrations of lignin and 200 sets with that of N. When the original paper did not provide climate data, Temperature (here refer to mean annual temperature, MAT, the same after, °C) and Precipitation (here refer to annual precipitation, APT, the same after, dm) values were taken from Müller's (1982) climate collection on the basis of the geographical co-ordinates.For stands with weather stations at greater distance than 1 degree in latitude or longitude, climatic data were interpolated among surrounding weather stations.

Data and Data Processing
The first-year mass loss (FML) values ranged from 10.0 to 100% with N concentration ranging from 0.1 to 4.8% and those of lignin from 4 to 50%.Temperature ranged from -1.7 to 30.2 °C and Precipitation from 4.43 to 30.4 dm.The average value for N was 0.49% for coniferous and 1.15% for broadleaf litter.With standard errors (SE) of 0.02 and 0.06, respectively, they were significantly different.For lignin concentration, the average value was 29.1% for coniferous and 17.9% for broadleaf litter, which were significantly different (p < 0.001) (Table 1).The distribution of data within each of the variables is seen in Fig. 1.
We subdivided the data in a first step into the categories broadleaf and coniferous litter.Further we divided 'broadleaf' into the subgroups 'deciduous broadleaf' and 'evergreen broadleaf'.At genus level, we analyzed the separate genera Pinus (pine), Picea (spruce), Quercus (oak) and subdivided Quercus into deciduous and evergreen.
With natural-log transformed FML, we calculated simple and multiple regressions between FML and Temperature and Precipitation.We used linear and exponential regressions to describe the effects of N and lignin concentrations on FML.We used the software SigmaStat (SPSS 1997).
To determine relative influences on FML, data for Temperature, Precipitation, and N were transformed using the program Standardize Transform (SPSS 1997).The standardized variables are dimensionless with a mean of zero and a standard deviation of 1.0.Thus, in a multiple regression equation, the values of the coefficients indicate their contributions to the variation in FML.In order to show the differences in the effect of Temperature, Precipitation and N on FML in an equation, t-test was applied to test if a significant difference exits between the coefficients of these independent variables.A similar test was also made on the effect of Temperature (or Precipitation, and N) on FML between the equations representing different litter groups.
The fit of regression equations was assessed with the coefficient of determination (R 2 ).The adjusted coefficient of determination (R 2 adj ) allows us to compare the goodness of model fit by taking into account the number of samples used (Ekbohm and Rydin 1990).We used t-test to determine the difference between the coefficients of independent variables within a multiple regression equation and between the coefficients of independent variables in pairs of equations.

Mass Loss of Different Foliar Litter Types in Relation to Climatic Factors
For all data combined (broadleaf plus coniferous litter), R 2 adj was 0.407 with Temperature and Precipitation as independent variables (Table 2).For broadleaf litter, R 2 adj became 0.307 and for coniferous R 2 adj was 0.124.Broadleaf and coniferous litter as separate groups both had significant linear relationships (p < 0.001) between FML, Temperature and Precipitation as independent variables in single or multiple regressions (Table 2, Fig. 1).
There was a higher variation among FML values for broadleaf foliar litter samples than for coniferous (Fig. 1).Broadleaf foliar litter generally had higher FML under the same climatic conditions as compared with coniferous litter.Thus, maximum FML reached 100% for broadleaf litter at a Temperature of 15 °C and above and at a Precipitation of 15 dm, but only c. 60% for coniferous litter at the same Temperature and Precipitation (Fig. 1).
Similar to broadleaf and coniferous litter, the groups 'deciduous broadleaf' and 'evergreen broadleaf' litter were highly significant (p < 0.001) for the relationships between FML and the climatic factors (Table 2, Fig. 2).Evergreen broadleaf litter had a clearly better relationship to Temperature and Precipitation (R 2 adj = 0.526) than deciduous broadleaf with R 2 adj = 0.147 (Table 2).However, under the same climatic conditions, there was almost no difference in FML between litter of evergreen broadleaf and deciduous broadleaf although we found more data for evergreen at warmer and wetter sites (Fig. 2).
There was a positive relationship between FML and Temperature for Pinus (p < 0.001) but not with any of the other genera (Table 3, cf Fig. 3).For Precipitation there were highly significant relationships for Picea, Quercus, and evergreen Quercus (Fig. 3) with p = 0.001 (Table 3).For Pinus the p value approached significance (p < 0.100) but for deciduous Quercus, there was no significance to Precipitation (Table 3).
We found a clear variation among genera as regards the significance of the relationship between FML and the combined Temperature and Precipitation.Thus, for Pinus the R 2 adj was 0.109 (p = 0.003) and for Picea R 2 adj was 0.273 (p = 0.036).The model for combined Quercus was better with R 2 adj = 0.352 (p < 0.001).The model for the subgroup evergreen Quercus gave a R 2 adj of 0.635 (p < 0.001), whereas that for deciduous Quercus was not significant (Table 3).

Mass Loss of Different Foliar Litter Groups and Genera in Relation to Litter Quality
For coniferous and broadleaf litter, both separately and combined, the relationships between FML and N concentration were highly significant in both linear and exponential models (p < 0.001), but the fits were better in the latter with R 2 adj = 0.408 for all litter, 0.173 for coniferous and 0.210 for     broadleaf litter in comparison with the linear model (R 2 adj = 0.265 for all litter, 0.154 for coniferous and 0.131 for broadleaf litter) (Fig. 1, Tables 4 and 5).
For evergreen broadleaf litter, FML varied significantly with N in linear (R 2 adj = 0.187) and exponential models (R 2 adj = 0.261), both at p < 0.001, with a better fit for the latter (Tables 4 and 5).For deciduous broadleaf litter both models were significant, but the exponential model gives a better fit (Tables 4 and 5).
For the genus Pinus there was a positive relationship (p < 0.001) between FML and N as a single factor and for evergreen Quercus with p < 0.05 in both a linear (Table 4) and an exponential model (Table 5).For the genera Picea and deciduous Quercus there was no significance for N as a single factor.
Lignin concentration for coniferous litter ranged from c. 20 to 40%, and for broadleaf litter from c. 4 to 50% (Fig. 1).For all litter combined as well as for coniferous and broadleaf separately, lignin was not significant as a single substrate-quality factor   and there was no trend indicating that FML was influenced by initial lignin concentration (Figs. 1 and 2).This was also seen for deciduous and evergreen broadleaf litter.Neither for the separate genera was lignin significant as a single factor and there was no clear trend that FML was influenced by lignin concentration (Figs. 3 thru 5).

Combined Effects of Climatic and Litter-Quality Variables on First-Year Mass Loss
The multiple linear regression models of FML against Temperature, Precipitation, and N were highly significant (p < 0.001) for the main groups, namely all litter types combined, broadleaf, coniferous, evergreen broadleaf, and deciduous broadleaf (R 2 adj = 0.702 to 0.204) with p < 0.001.For most genera we found highly significant models with R 2 adj = 0.223 for Pinus, 0.626 for Quercus and 0.749 for evergreen Quercus.Deciduous Quercus gave a significant relationship (p = 0.038; R 2 adj = 0.540) whereas the litter of Picea did not (p = 0.093 and R 2 adj = 0.221; Table 6).For Quercus evergreen the R 2 adj even reached 0.749 explaining about 75% of the mass loss in the first year and for broadleaf evergreen 70%.
In these models, describing the combined effects of climatic factors and N, Temperature had a negative effect on FML for the groups 'broadleaf litter', 'Quercus' and 'deciduous Quercus', Precipitation had a negative effect for Pinus, and both Temperature and N had a negative effect for Picea (Table 6).In none of these cases was the effect significant.

Relative effects of Annual Average
Temperature, Annual Precipitation, and N on First-Year Mass Loss By using standardized climatic and litter-quality factors and FML we found (Table 7) that the effects of Temperature, Precipitation, and N on FML in relative units were different among the groups of litter types and among genera.For all litter combined ('All litter'), the effect of Precipitation was significantly larger (p < 0.001) than those of Temperature and N (Table 7).In fact, Table 6.Linear regressions of first-year mass loss of leaf litter (ln(FML)) against mean annual temperature (MAT, °C), annual precipitation (APT, dm), and initial litter nitrogen (N,%) concentration for broadleaf and coniferous litter combined (All litter), the separate groups coniferous and broadleaf, as well as deciduous broadleaf (Dec Br) and evergreen broadleaf (Evergr Br) and the genera Pinus, Picea, and Quercus, the latter also subdivided into deciduous Quercus  For deciduous Quercus and Pinus the significance level was p = 0.05.Between functions we tested the coefficients of two variables of paired equations.1) Significant differences (p < 0.001) were found between the groups coniferous and broadleaf as regards MAT and APT and at p < 0.01 for N. 2) Significant differences (p < 0.001) were found between deciduous and evergreen broadleaf litter as regards Intercept, MAT and APT.
3) Significant differences (p < 0.001) were found between Pinus and Picea for Intercept, MAT and N. 4) Significant differences were found between deciduous and evergreen Quercus litter (p < 0.001) as regards Intercept and MAT and at p < 0.01 for N.
the coefficient for Precipitation was c. 10 times that of Temperature.For the group 'coniferous' there were no significant differences, whereas for broadleaf litter there was a clearly higher effect of Precipitation.Thus was the effect of Precipitation for broadleaf litter significantly higher than both that of Temperature, which was negative, and N. The same pattern was seen for the separate groups of both deciduous and evergreen broadleaf and Quercus and the negative coefficient for Temperature was even more emphasized.Evergreen Quercus had a positive sign for Temperature but followed a pattern with significantly higher influence of Precipitation than of Temperature and N. Deciduous Quercus had a clearly negative coefficient for Temperature (-0.425) and it was significantly lower than the coefficient for Precipitation (p < 0.001) and significantly lower than that for N (Table 7).
Pinus had a somewhat different pattern with a significant difference between a positive Temperature and a negative Precipitation, whereas there was no significant difference between coefficients for Temperature and N.For Picea there was no significant difference between the coefficients.For pairs of equations there were significant differences between the coefficients of the same variable.Thus, there were significant differences between the groups 'coniferous' and 'broadleaf' as regards all Temperature, Precipitation and N (Table 7).Further, there were significant differences (p < 0.001) between deciduous broadleaf and evergreen broadleaf for Temperature and Precipitation and between Pinus and Picea as regards Temperature and N (p < 0.001).There was also a significant difference between deciduous and evergreen Quercus (p < 0.001) as regards Temperature and at p < 0.01 for N.

First-Year Mass Loss at 100%
Several measured FML values reached 100%.The litter species with so high a mass-loss rate were broadleaf (mainly deciduous) and found in climates with Temperature in the range 14 to 28.1 °C and Precipitation between 14 and 28.2 dm (Fig. 1, Appendices A and B).The substrate chemistry ranged for lignin concentration between 10.8 and 22.4% and N concentrations between 0.94 and 3.1%.

Differences in Variation of FML As
Related to Climate and Litter-Quality Variables for Different Groups of Foliar Litter Our comparison was conducted at four levels, (i) broadleaf vs. coniferous litter, (ii) deciduous broadleaf vs. evergreen broadleaf litter, (iii) genus level and (iv) within a genus (deciduous Quercus vs. evergreen Quercus).To our knowledge, such analyses of decay response have not been carried out in earlier work.
The clearly different responses among the groups to Temperature, Precipitation and N indicate different decomposition patterns among genera and groups of litter as regards temperature and precipitation regimes.We may thus note that only the decomposition of Pinus was promoted by Temperature (Table 3), whereas the other litter types were not.For Picea that was observed by Berg et al. (2000) in a climate gradient.

Effects of the Different Variables on First-Year Mass Loss of Leaf Litter -Implications for Climate Change
Climate affects the chemical composition of newly shed litter (Aerts 1997, Liu et al. 2006).
Litter chemical composition as well as temperature and moisture in their turn influence the microbial activity.With an increase in annual average temperature, leaf litter N concentration increases at a regional scale (Liu et al 2006).The general acceptance is that climatic factors and litter quality play dominant roles on mass-loss rates along a broad climate gradient.Still, we may see that Temperature, Precipitation and N create a complicated pattern with very different responses among litter types and genera.
Our findings have two aspects of important implications.First, the changing of both Temperature and Precipitation will greatly influence FML; but with the changes of the same relative unit in Temperature and Precipitation, they displayed evidently different effects on FML, and in some cases the difference was significant (Table 7).This means that with global warming, we need to consider different effects of temperature and precipitation on FML.Second, the effects of Temperature, Precipitation, and litter quality on FML varied among groups of litter types.When using standardized variables (Temperature, Precipitation, and N) in multiple regressions, we found that the coefficients of standardized Temperature, standardized Precipitation and standardized N were 0.327, 0.061, and 0.199, respectively, for the coniferous model, showing that the effect of Temperature was much stronger than for Precipitation, but -0.032, 0.802 and 0.156, respectively, for the broadleaf model, suggesting that on a large scale and over several species the effect of temperature on FML may be negative or at least very close to zero.A clear indication is that on a large scale there is a strong difference in decomposition dynamics between coniferous and broadleaf litter with the decomposition of the former being more sensitive to temperature and relatively little to precipitation.We may note that the climate regions for these two groups are different for the majority of data and that the coniferous litter as a group has a somewhat shorter range in Temperature as compared to broadleaf litter and that the same applies to Precipitation (Fig. 1).Such differences in response to climate variables may result in corresponding very different responses among forests to climate change.Thus the initial decomposition of Pinus needle litter would be stimulated by an increasing temperature but that of Picea not.
Even within a genus, viz. between deciduous Quercus and evergreen Quercus, a clear difference was found between the coefficients.Thus were the coefficients of standardized (Temperature), standardized (Precipitation) and standardized (N) -0.425, 0.701, and 0.435, respectively, for deciduous Quercus, and 0.249, 0.768 and 0.255, respectively, for evergreen Quercus.A reasonable conclusion would be that as seen over a larger region, litter with properties that appear to be generated by local climate would not necessarily behave according to traditional and postulated patterns.
Generally, higher temperature means a longer period during which microbes can decompose litter (Liski et al. 2003).The effects described relate to the mass loss in the first year.Thus, the relative influence of changed Precipitation, Temperature and N relate to part of the decomposition process but it has been shown (Johansson et al. 1995) that in partially decomposed Scots pine needle litter the rate was so strongly controlled by the concentrations of lignin which increase in the decomposition process that the effect of temperature was negligible.That was in the temperature range of -1.0 to +10.0 °C.

Fit of Regression Models
When Meentemeyer (1978) investigated the effect of using annual evapotranspiration (AET), lignin concentration and the quotient AET-to-lignin as an interaction term, he found that AET alone accounted for 51% of the variance in observed decay rates, AET/lignin concentration added 19% and lignin concentration added 2% of the total (72%) variance accounted for.
Using an index which combined Temperature and summer drought based on only some temperature variables, Liski et al. (2003) could explain the first-year mass loss with an R 2 value of about 0.7 for Scots pine needle litter at a regional scale.When combined into a multiple regression, Temperature, Precipitation, and lignin-to-N ratio explained 73% of the variance in mass remaining for all sites and tissues (Moore et al. 1999).In the present study, R 2 adj reached a similar level (0.7) when climatic and litter-quality variables were employed as independent variables in multiple regression models, for single species even above 0.8 (Tables 6 and 7).

First-Year Mass Loss vs Possible Carbon Sequestration
With 100% mass loss of the leaf litter in one year or less and the assumption of one leaf generation per year, no remaining mass from foliar litter would accumulate on the forest floor and form an organic layer that sequesters carbon.Foliar litter is a major litter component and may determine the sequestration rate (cf.Berg et al. 2000).This means that any possible sequestration that would take place from the leaf litter component would be in the form of resistant compounds leached with water and precipitated in the mineral soil.
No sequestration would take place to allow the formation of e.g. an O horizon.The litter species with so high a mass-loss rate were broadleaf (mainly deciduous) and found in subtropical and tropical climates with Temperature in the range 14 to 28.1 °C and Precipitation between 14 and 28.2 dm (Fig. 1, Appendices A and B).With these climate conditions and lignin concentration ranging between 10.8 and 22.4% and N concentrations between 0.94 and 3.1% we may distinguish a niche in which no sequestration takes place.Our reasoning does not mean that these litter types would be the only ones that do not sequester carbon in the form of a humus layer but rather that they would be litter types that clearly do not form any such layer.We found 18 cases with such a high mass-loss rate.A main species that is found in this group is Quercus.Eleven further cases with mass loss between 95 and 100% included litter from the genera Populus and Shorea.In a given forest there may of course be other litter components from these species that sequester carbon.

Concluding Remarks
The differences in response of different species and types to different influencing factors (annual average temperature, annual precipitation and substrate quality) create a considerably more complicated pattern among litter species on a regional level than what has been expected.It thus appears that the response in decomposition to changes in the climate should be followed at least at the level of genus, possibly species.An ecological niche at which no carbon sequestration takes place in a humus layer encompassed subtropical and tropical broadleaf species.

Table 1 .
Average concentrations of nitrogen and lignin for the litter groups coniferous, broadleaf, evergreen broadleaf (Evergr Br) and deciduous broadleaf (Dec Br) as well as significant differences.

Table 2 .
Linear regressions of the first-year mass loss of foliar litter (FML) against the climatic factors mean annual temperature (MAT, °C) and annual precipitation (APT, dm) for broadleaf and coniferous litter types combined (All litter), as well as coniferous, broadleaf, deciduous broadleaf (Dec.Br) and evergreen broadleaf (Evergr.Br) litter as separate groups.Standard error (SE) is given.

Table 3 .
Linear regressions of first-year mass loss of foliar litter ln(FML,%) against mean annual temperature (MAT, °C), annual precipitation (APT, dm) for the genera Pinus, Picea and Quercus as well as for the subgroups evergreen Quercus (Evergr Qu) and deciduous Quercus (Dec Qu).Standard error (SE) is given.

Table 5 .
Exponential regressions of the first-year mass loss of foliar litter (FML) against initial litter nitrogen (N) concentration (%) as litter-quality factor for broadleaf and coniferous litter combined (All litter), as well as for the separate groups of coniferous, broadleaf, deciduous broadleaf (Dec Br), evergreen broadleaf (Evergr Br), the genera Pinus, Quercus, and Quercus subdivided into deciduous Quercus (Dec Qu) and evergreen Quercus (Evergr Qu).The equation used was FML = A × (1 -exp(-B × N)).a) For Picea the coefficients were not listed here because no model matched the data.

Table 7 .
Summary of regressions of standardized first-year mass loss (Stand(FML), %) against standardized mean annual temperature (Stand (MAT), °C), annual precipitation (Stand(APT), dm) and standardized litter nitrogen concentration (Stand (N), %) for combined broadleaf and coniferous litter (All litter), for the separate groups coniferous, broadleaf, deciduous broadleaf (Dec Br) and evergreen broadleaf (Evergr Br) as well as the genera Pinus, Picea, Note: Tests for significant differences were made both within and between functions.Thus within an equation, different letters after the coefficients of Stand(MAT), Stand(APT) and Stand (N) indicate a significant difference.The levels of significant difference (t-test) are p < 0.001 for All litter, broadleaf, deciduous broadleaf, evergreen broadleaf, Quercus, and evergreen Quercus.
Data set for the first-year mass loss of leaf litter in Eurasian forests compiled based on the publications listed in Appendix B. Abbreviations: E, evergreen; D, deciduous; longit., longitude; latit, latitude; altit, altitude; temp, mean annual temperature; preci, annual precipitation; N, nitrogen.
Appendix A.