European beech deadwood can increase soil organic carbon sequestration in forest topsoils

Forest Ecology and Management 405 (2017) 200–209

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European beech deadwood can increase soil organic carbon sequestration in forest topsoils

MARK

⁎

Janna Wambsganss1, Kenton P. Stutz , Friederike Lang Chair of Soil Ecology, Institute of Forest Sciences, University of Freiburg, D-79085 Freiburg, Germany

A R T I C L E I N F O

A B S T R A C T

Keywords: Coarse woody debris Forest management SOM stability Soil aggregate Density fractionation

Deadwood plays a crucial role in forest ecosystems, yet its impact on soil properties and specifically soil organic matter (SOM) stabilization is hitherto not fully understood or studied. We hypothesized that downed deadwood would enhance the light, labile SOM fraction in forest topsoils, and that those changes would be enhanced by advanced decay and higher rates of soil bioturbation that would move deadwood fragments into mineral soil. To test our hypotheses, we took topsoil samples directly next to European beech (Fagus sylvatica L.) downed deadwood and samples from paired reference points at eight stands in Southwest Germany. From those samples we separated SOM into three density fractions linked to physical and chemical SOM stabilization processes: the free light fraction, the aggregate-occluded light fraction and the mineral-adsorbed heavy fraction. On silicate bedrock, deadwood increased the free light fraction by 57% (6.0 ± 4.2 mg g−1) compared to reference points. In contrast on calcareous bedrock, deadwood decreased the free light fraction by 23% (9.0 ± 3.5 mg g−1) compared to reference points. Deadwood with advanced decay from all sites increased the aggregate-occluded light fraction by 40% (3.7 ± 1.1 mg g−1) as well as total soil organic carbon (SOC) stocks by 24% (12.8 ± 4.5 mg cm−3) as compared to reference points. In summary, the light fraction of SOM was affected by deadwood depending on site conditions and the more stable, aggregate-occluded fraction eventually increased near decayed deadwood through interactions between stimulated biological activity and both particulate and dissolved organic matter. Altogether these results indicate that deadwood increases SOC stocks at sites where SOM decomposition is slow enough to enable occlusion of particulate organic matter within aggregates.

Introduction Deadwood—downed woody debris, snags or stumps—is a characteristic feature of unmanaged forest ecosystems that supports multiple services, especially through biodiversity (Harmon et al., 1986). However, in comparison to unmanaged forests deadwood is relatively scarce in managed Central European forests (Ministerial Conference on the Protection of Forests in Europe, 2015) where it represents only a small fraction of the forest floor. Given the importance of and global threats to biodiversity in sustaining environmental services (Ceballos et al., 2015), foresters have up till now managed deadwood stocks and type to enhance biodiversity balanced against associated risks and hazards (Lachat et al., 2013). Other services provided by deadwood are rarely considered in management strategies because they are either assumed to be negligible or past research has been insufficient and

inconclusive (Stutz and Lang, 2017). One such service hitherto underresearched is sequestration of carbon originating from deadwood (Magnússon et al., 2016). Decomposition of deadwood is dominated by fragmentation, dissolution and respiration (Harmon et al., 1986). During respiration, C is lost as CO2 to the atmosphere, whereas dissolved organic material and wood fragments either remain in place or have the potential to move horizontally or vertically. Specifically leachates from deadwood can enter soil through percolating water, while fragmented particulate organic material (POM) can enter topsoil through bioturbation as a result of biological activity—Ma et al. (2014) found more POM deeper in soil when soil-dwelling earthworms were more abundant. Despite these potential processes of adding C to soil, no increases in soil organic carbon (SOC) concentrations or stocks as a result of deadwood have often been reported and attributed to deadwood being inert until C was

Abbreviations: fLF, free light fraction; oLF, aggregate-occluded light fraction; HF, heavy fraction; POM, particulate organic matter; WEOC, water-extractable organic carbon; SUVA280, specific ultraviolet absorbance at 280 nm; MAP, mean annual precipitation; MAT, mean annual temperature ⁎ Corresponding author. E-mail addresses: [email protected] (J. Wambsganss), [email protected] (K.P. Stutz), [email protected] (F. Lang). 1 Present address: Chair of Silviculture, Institute of Forest Sciences, University of Freiburg, D-79104 Freiburg, Germany. http://dx.doi.org/10.1016/j.foreco.2017.08.053 Received 4 July 2017; Received in revised form 25 August 2017; Accepted 27 August 2017 0378-1127/ © 2017 Elsevier B.V. All rights reserved.

Forest Ecology and Management 405 (2017) 200–209

Summer 2015 Regional freshwater limestones. Triassic sandstones.

1. How do SOM fractions linked to different degrees of stability change under downed deadwood as compared to reference points with regular forest floor litter? 2. How do soil ecosystem- and deadwood-specific properties (i.e., soil fauna and deadwood decay) affect the impact of downed deadwood on SOM stability fractions? To answer these questions, we measured the distribution of OC among SOM stability pools at test points directly next to downed deadwood logs and at reference points that were assumed to not be influenced by deadwood. We tested the following hypotheses:

b

a

Summer 2015 90

85 8.8

8.4 950

900 400

500 Moder

Moder Cambisol

Medium sand Cambisol Buntsandsteinb (silicate)

Kieselsandsteinb (silicate) 9° 26′22″E, 48° 43′57″N Schachen

Wartenberg

lost to aboveground respiration (Spears and Lajtha, 2004; Krueger et al., 2017). However, multiple studies have reported that deadwood changes the quantity and composition of organic residues entering the soil, which can impact to soil functioning. Specifically increased fluxes of dissolved organic carbon (DOC) derived from decaying wood have been observed (Hafner et al., 2005; Kuehne et al., 2008; Kahl et al., 2012). Several studies also found stronger effects on soils (e.g., higher DOC concentrations) from deadwood in advanced decay compared to deadwood with less decay (Kuehne et al., 2008; Gonzalez-Polo et al., 2013). Likewise elevated concentrations of soil organic matter (SOM) in mineral topsoil under deadwood in advanced decay stage were measured by Krzyszowska-Waitkus et al. (2006). Moreover, the compositional quality of deadwood-derived decay metabolites and the resulting SOM differ from leaf litter-derived SOM. Spears and Lajtha (2004) found that dissolved organic matter (DOM) derived from deadwood was significantly richer in polyphenols than DOM originating from regular forest floor litter. Krzyszowska-Waitkus et al. (2006) correspondingly found 60–70% higher contents of phenolic compounds along with higher C/N ratios in the organic layer under deadwood. And Stutz et al. (2017) linked tree species-specific changes in soil influenced by deadwood to the composition of leached phenolic matter. The altered quantity and composition of organic matter added to the soil by deadwood as observed by several studies could also affect the rate at which SOM is mineralized and returned to the atmosphere. The persistence and fate of SOM and thereby organic C (OC) is governed by physical, chemical and biochemical mechanisms that limit access to decomposing organisms (Sollins et al., 1996; von Lützow et al., 2006; Dungait et al., 2012). Through density fractionation, SOM can be separated into three fractions associated with these stabilizing mechanisms and thereby functional pools that are characterized by different degrees of stability, i.e., resistance against mineralization, and consequently residence times in soil (von Lützow et al., 2007; Marschner et al., 2008). These fractions include two light fractions (LF): one consisting of free particulate organic matter—the active pool with relatively short residence times of C—and a second consisting of physically stabilized aggregate-occluded particulate organic matter—the intermediate pool. The third, the heavy fraction (HF) comprises the chemically stabilized mineral-associated organic matter—the slow or passive SOM pool with the longest C residence times (von Lützow et al., 2008). While the mineral-associated SOM pool is relatively stable due to its high resistance against mineralization, the light fraction pools have been shown to be more sensitive to changes in land use (Bremer et al., 1994) and altered litter inputs (Martens, 2000; Grüneberg et al., 2013). To the best of our knowledge, the meso-scale impact of deadwood on SOM stability pools has not yet been investigated. Only a recent review by Magnússon et al. (2016) argued that impacts of deadwood on SOM stabilization and thereby long-term C sequestration in forest soils could be substantial. Crucially, increased stability of SOM would have the potential to enhance overall C sequestration in forests. Given the knowledge gaps concerning the contribution of deadwood to SOM stabilization, we address the following questions:

Silt loam

Autumn 2014

Summer 2015 90

60 7.3

8.0 1100

1490 800

540 Moder

Moder Coarse sandy loam

Loamy sand

Cambisol

Cambisol

Paragneis (silicate)

Buntsandsteinb (silicate)

7° 57′50″E, 48° 1′20″N 7° 55′58″E, 49° 16′59″N 7° 47′6″E, 49° 14′30″N Hahnenkopf

Cambisol Paragneis (silicate) Sternwald

Kappeltal

Conventwald

Spring 2015

Spring 2015 80 8.2 1100 580 Mull

Spring 2015

Cambisol

Sandy loam

80 6.6 1300 900 Mull

Summer 2015

Migmatite (silicate)

Sandy clay loam

80

85 7.1

7.5 750

860 580

700 Mull

Mull Clay

Silt clay loam

Rendzic Leptosol

Rendzic Leptosol Süsswasserkalkea (calcareous)

Season sampled Percent beech (%) MAT (°C) MAP (mm) Elevation (m) Forest floor Texture class Soil group

Bankkalke (calcareous) Siebter Fuß

Teutschbuch

10° 8′30″E, 48° 43′34″N 9° 27′40″E, 48° 11′50″N 7° 53′34″E, 47° 55′34″N 7° 52′30″E, 47° 58′00″N

a

Bedrock (type) Coordinates (WGS84) Study site

Table 1 Study sites, season sampled, coordinates, bedrock, soil reference group and texture class (IUSS Working Group WRB, 2014), elevation, mean annual precipitation and temperature (MAP and MAT, respectively), and visually estimated proportion of beech basal area for the eight stands (Stutz and Lang, 2017). Mull forest floor has no Oa horizon while moder forest floor has an Oa horizon.

J. Wambsganss et al.

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aggregate-occluded light fraction (oLF) and the heavy fraction (HF). The procedures of Golchin et al. (1994) and Graf-Rosenfellner et al. (2016) were followed using a sodium polytungstate (SPT; Sometu, Berlin, Germany) solution with a density of 1.6 g cm−3 for the separation of 20–25 g bulk soil samples into the two light fractions (material with ρ < 1.6 g cm−3) and the HF (material with ρ > 1.6 g cm−3). First, the fLF was separated by centrifugation (26 min at 3500 rpm) and filtered >1.5 μm (VWR C-free glass microfibers filter 696, Leuven, Belgium). Second, the oLF, which is assumed to contain C enclosed in stable aggregates, was released by sonic disruption of soil aggregates at an energy level of 400 J ml−1 using a Vibra Cell high intensity ultrasonic processor (Sonics and Materials, Newton, Connecticut, USA) with a 13 mm diameter titanium tip and 60% applied amplitude, and separated in the same manner as the fLF; the energy applied by the ultrasonic processor was calorimetrically calibrated (North, 1976). The residual, denser material was classified as the HF and was assumed to include all mineral-bound OC. The SPT solution was washed from each fraction using high-purity water until the electric conductivity of the suspensions reached 50 μ S for the light fractions and 200 μ S for the heavy fraction. All recovered density fractions were desiccated through freeze-drying and subsequently dried at 105 °C. Mass recovery efficiency was on average 95.08 ± 0.88% and total OC recovery efficiency was 93.13 ± 1.85%. The proportion of OC (%) belonging to i fraction was calculated as OCi (%) = OCi (mg)/ OCrec (mg)·100 , where OCrec is the total OC recovered after fractionation. Each bulk soil sample and density fraction was milled and combusted at 1150 °C (Elementar Vario EL Cube) to determine total C concentrations and C/N ratios (Nelson and Sommers, 1996). Total C was assumed to be OC at the six silicate sites. For the two calcareous sites, inorganic C was determined for the HF and bulk soil samples by removing OC at 550 °C for 5 h in a muffle furnace. Total SOC stocks were calculated from bulk SOC concentrations and soil bulk densities based on the dry mass (105 °C) of single, 100 cm3 structured soil rings per sampling point (Blake and Hartge, 1986); we assumed each soil ring was representative of soil physical properties to a depth of 10 cm. Furthermore, water-extractable OC (WEOC) and aromaticity, pH and porosity were measured for all bulk soil samples. From non-milled samples, WEOC (1:2 soil to solution ratio) was extracted for 24 h, filtered <0.45 μm (Sartorius Stedim Biotech cellulose nitrate filter, Göttingen, Germany) and analyzed by thermal oxidation (Multi N/C 2100S analytic jena) according to Gutachterausschuss Forstliche Analytik (2014, A3.2.2.1). Aromaticity of WEOC was measured as the specific ultraviolet absorption at 280 nm (SUVA280; Perkin Elmer’s UV VIS Spectrometer, Model Lamda 2) divided by the OC concentration (Weishaar et al., 2003); pH was not buffered. Soil pH and porosity were measured as in Stutz and Lang (2017) through soil water extracts (Metrohm 751 GPD Titrino) and vacuum pycnometry of 100 cm−3 soil rings (Danielson and Sutherland, 1986), respectively.

1. The light fraction, the most labile pool, is more sensitive to deadwood effects than the heavy fraction, the most inert pool. 2. The rate of soil bioturbation and decay class of deadwood regulate the impact of deadwood on SOM stabilization in the following manner: (a) deadwood on soil with characteristically high levels of bioturbation impact SOM stability pools to a greater extent than deadwood on soil with less bioturbation, and (b) deadwood in advanced decay stages impact SOM stability pools more strongly than less decayed deadwood. Materials and methods Study sites Soil samples were taken from eight European beech (Fagus sylvatica L.) stands in Southwest Germany; they are the same samples as used in Stutz and Lang (2017). Location, soil and stand properties, and season sampled are listed in Table 1. All sites were sampled before leaf senescence. Field design At each study site, four downed deadwood logs of European beech (Fagus sylvatica) were selected and, from the center of each log, paired soil samples—a test (deadwood) sample and reference (control) sample 2–3 m removed—from the Ah (0–10 cm) horizon were taken simultaneously. Selected logs had a minimum length of 1.8 m, a diameter ⩾15 cm (maximum was 65 cm with a mean of 32 cm) and sapwood affected by white-rot. Logs with different extents of decay were selected and decay classes were based on the “pocket-knife” method described in Table 2 (Lachat et al., 2014); decay class 1 was excluded for not being present long enough to influence soil. Decay classes did not differ between mull and moder sites, nor between calcareous and silicate bedrocks; diameter likewise did not differ between those categories, nor between decay classes. Each logs’ position was longitudinal to the slope in order to avoid excessive accumulation of litter material and moisture on one side of the logs. Consequently, we assume the input of leaf and fine litter at paired points has been the same with minimal micro-climatic differences. We also assume seasonality of sampling did not affect the relationship between paired deadwood and control points due to deadwood’s multiannual influence on soil. Due to a relatively high stone content (inorganic solid material having a diameter > 2 mm) at the study site Conventwald, only three deadwood logs could be sampled. Laboratory analysis Soil samples were air-dried at 40 °C and sieved < 2 mm to separate fine earth from coarse material (i.e., stones and coarse roots) before laboratory analysis. For each sample, SOM was separated through density fractionation into three C pools: the free light fraction (fLF), the

Statistics Absolute differences in SOM density fractions and soil properties between paired deadwood and control points were calculated using the following equation (Stutz et al., 2017):

Table 2 Decay class characteristics and features differentiated by use of a pocket knife (Lachat et al., 2014). The number of sampled stems is reported as n. Decay class (n)

Characteristics and features

1 (0) 2 (8)

Fresh with green cambium Hard without sap and pocket knife hardly penetrating with fibers Softer with pocket knife penetrating easily with fibers, but not across Soft with pocket knife penetrating easily both with and across fibers Loose material and mostly disintegrated

3 (14) 4 (8) 5 (1)

Δ(i) = Deadwood (i )−Control (i)

(1)

Likewise, relative differences in SOM density fractions and soil properties between paired deadwood and control points were calculated as the absolute difference divided by the control values (Stutz et al., 2017):

Δ%(i) =

Δ(i) ·100 Control (i)

(2)

Standard errors were calculated for all mean values. Differences between deadwood and control points were tested for significance 202

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Influence of site characteristics For both forest floor types, neither OC concentrations nor proportions of any density fraction differed significantly between deadwood and control points (Fig. 3a). Despite no changes in those pools, significant differences between deadwood and control points were found for WEOC and porosity, but only at moder sites. At those sites, WEOC concentrations and porosity were 62 ± 29 mg L−1 and 6.2 ± 1.9% higher at deadwood points compared to control points, respectively (Fig. 3a). Also, only Δ% porosity differed significantly between mull and moder sites (Wilcoxon, p < 0.01). For both calcareous and silicate bedrocks, fLF-OC concentrations differed significantly between deadwood and control points (Fig. 3b). Compared to paired control points, deadwood fLF-OC concentrations were significantly enhanced (+ 6.0 ± 4.2 mg g−1) at sites on silicate bedrock and, in contrast, significantly reduced (−9.0 ± 3.5 mg g−1) at sites on calcareous bedrock. Furthermore, significantly higher C/N ratios (+ 4.3 ± 1.9%) and higher porosity (+ 8.2 ± 2.6%) were measured for deadwood points compared to control points only at silicate sites. Additionally, Δ% fLF, total OC and porosity differed significantly between calcareous and silicate bedrock (Wilcoxon; p < 0.05, p < 0.05 and p < 0.01, respectively). Fig. 1. Mean proportions of total OC for each SOM fraction by deadwood and control points (n = 31); error bars represent one standard error of mean percentage of total OC for each fraction. Numeric values show OC concentrations (mg g−1) for each fraction.

Influence of deadwood characteristics Only deadwood with advanced decay (class 4) had significant differences in SOM density fraction proportions and concentrations of OC between deadwood and control points. Specifically, deadwood HF constituted significantly less of total SOC compared to control points (LME, p < 0.05). Additionally, oLF-OC concentrations were significantly higher at decay class 4 deadwood points than control points (+ 3.7 ± 1.1 mg g−1; Fig. 3c). Total SOC stocks were also significantly elevated at decay class 4 deadwood points compared to control points (+ 12.8 ± 4.5 mg cm−3). Significant differences in other measured soil properties were found as well, again almost exclusively for deadwood in decay class 4. Advanced decayed deadwood points had significantly elevated WEOC concentrations (+ 62 ± 25 mg L−1) and aromaticity (SUVA280,+0.0018 ± 0.0007 L mg−1 cm−1 of C) in comparison to control points (Fig. 3c). An exception was elevated C/N ratios at moderately decayed deadwood points in comparison to control points (+ 0.87 ± 0.37 %; Fig. 3c).

through linear mixed effects (LME) models with each study site and log included as nested random factors. Differences in Δ%(i) between site and decay classes were checked with Wilcoxon signed-rank tests for two classes (forest floor type and bedrock) and Kruskal-Wallis tests for three classes (decomposition classes). For correlation analyses between deadwood and Δ values, Pearson’s correlation tests were used for normally distributed data and Spearman’s rank correlation tests for nonparametric data; negative values denote inverse correlations. ShapiroWilk test and Quantile-quantile plots were used to test for normality of the deadwood values. Significance levels were set at p = 0.05. All statistical analyses were performed with R Statistics 3.2.3 (2015).

Results Overall analysis of all sites

Correlation analyses For all samples regardless of site factors or decay class, no significant differences in density fraction proportions or concentrations were found between deadwood and control points. At both deadwood and control points the HF had the greatest share of the total OC followed by the fLF (Fig. 1). At control points for the two sites on calcareous bedrock, Siebter Fuß and Teutschbuch, the average total SOC concentration was 109.2 ± 5.9 mg g−1 with a stock of 74.7 ± 6.4 mg cm−3, C/ N of 12.82 ± 0.42%, pH of 6.65 ± 0.29, porosity of 74.5 ± 1.9% and a bulk density of 0.69 ± 0.05 g cm−3. In contrast, at the six silicate sites average SOC concentration was only 61.0 ± 7.1 mg g−1 with a stock of 57.9 ± 6.1 mg cm−3, C/N of 16.65 ± 0.33%, pH of 4.49 ± 0.10, porosity of 64.7 ± 1.6% and a bulk density 0.98 ± 0.04 g cm−3 (Fig. 2, Table 3). Mull and moder sites differentiated in a similar manner with mull control points having more OC, lower C/N ratios and bulk densities, and higher pH and porosity than moder control points (Table 3). Unlike for site factors, control points for each decay class were indistinguishable from one another save for lightly increasing SOC stocks (Table 3). Also, porosity and bulk density were highly correlated with one another for all samples (r = 0.989), and as such only porosity was further tested for differences between deadwood and control points when evaluated by site characteristics and decay classes.

A comparison of deadwood points for mull and moder sites showed distinct correlations for fLF-OC concentrations with other soil properties. Deadwood fLF-OC concentrations at moder sites had strong, significant correlations with total SOC stocks (ρ = 0.68, p < 0.01) and only weak, non-significant ones at mull sites (r = 0.06, p > 0.05). A similar pattern existed for correlations between fLF-OC concentrations and MAP (moder sites, ρ = 0.59, p < 0.05; mull sites, r = −0.27 , p > 0.05). Likewise, fLF-OC concentrations correlated strongly with total SOC stocks at silicate sites ( ρ = 0.53, p < 0.05) but not at calcareous sites (r = 0.032, p > 0.05), and significantly with MAP at silicate sites ( ρ = 0.48, p < 0.05) but not at calcareous sites (r = 0.22, p > 0.05). For decay class 4 deadwood samples, significant correlations between fLFOC concentrations and total SOC stocks ( ρ = 0.80, p < 0.05) were found as well as between HF-OC concentrations and total SOC stocks (r = 0.85, p < 0.05). In contrast, oLF-OC concentrations did not correlate with total SOC stocks (r = 0.08, p > 0.05) nor with any other property save deadwood diameter ( ρ = 0.77, p < 0.05). For Δ fLF-, oLF- and HF-OC concentrations, correlations were not always the same as with deadwood values. Similar to above Δ fLF-OC concentrations at moder and silicate sites correlated significantly with total SOC stocks (ρ = 0.59, p < 0.05; ρ = 0.51, p < 0.05; respectively) but not 203

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Fig. 2. Mean OC concentrations in the three density fractions across study sites, separately for deadwood and control points and bedrock type. The number of samples (n) is given for each control and deadwood class.

at mull and calcareous sites (r = 0.24, p > 0.05; r = 0.53, p > 0.05; respectively). Conversely Δ fLF-OC concentrations at calcareous sites correlated significantly with both MAP (ρ = −0.87, p < 0.01) and MAT (ρ = 0.87, p < 0.01), but not at all at silicate sites (MAP, ρ = 0.15, p > 0.05; MAT, ρ = −0.04, p > 0.05). As for decay class 4, neither Δ fLF-, oLF- nor HF-OC concentrations correlated significantly with any property.

based on whether the bedrock was silicate or calcareous, deadwood oLF increased only with advanced decay and deadwood HF had no observed changes. Additionally, deadwood with advanced decomposition had altogether higher total SOC stocks in the topsoil. An explanation following the interaction between the fLF, oLF, HF and deadwood along gradients of nutrient availability, biological activity and deadwood decay is described in the following subsections.

Discussion

Free light fraction The largest increase in Δ% for any density fraction was in the fLF on silicate bedrock; in contrast, the greatest decrease in Δ% for any density fraction was also in the fLF on calcareous bedrock. These results affirm hypothesis 1 that the fLF would be more sensitive to deadwood than the HF, at least in the topsoil. The overall high abundance of OC in the two light fractions is likewise comparable to topsoil in German beech forests (Grüneberg et al., 2014). However, we had also hypothesized that deadwood on soils with more bioturbation—i.e., sites with mull forest floor types as well as on calcareous bedrock—would lead to higher concentrations in either fLF, oLF or HF (hypothesis 2a). No such significant increases in any fraction

Impact of deadwood on SOM stabilization The lack of significant changes in the three density fractions as well as total SOC stocks between deadwood and control points across all eight study sites suggests that deadwood has no unequivocal influence on SOM stability and consequently OC sequestration. Yet, when categorized by underlying bedrock, forest floor type and decay class, a spectrum of changes between deadwood and control points were found in the density fractions corresponding to physical protection as well as overall SOC stocks: deadwood fLF concentrations either increased or decreased

Table 3 Mean deadwood and control values ( ± one standard error of the mean) for SOC stocks, C/N ratios, aromaticity (SUVA280 ), pH, porosity and bulk density by site factors and decay class. The number of samples is reported as n under Point type. Category

Point type (n)

SOC stock, mg cm−3

C/N ratio, %

WEOC, mg L−1

SUVA280, L mg C−1 cm−1

pH, −log10 mol H+ L−1

Porosity, %

Bulk density, g cm−3

Mull

Control (16) Deadwood (16)

65.8 ± 5.7 68.7 ± 4.7

14.30 ± 0.51 14.86 ± 0.64

416 ± 35 412 ± 35

0.0080 ± 0.0004 0.0085 ± 0.0004

5.78 ± 0.27 5.87 ± 0.27

71.2 ± 1.9 70.4 ± 1.7

0.80 ± 0.05 0.84 ± 0.05

Moder

Control (15) Deadwood (15)

58.9 ± 8.2 57.1 ± 10.8

17.11 ± 0.36 17.66 ± 0.41

242 ± 23 303 ± 22

0.0155 ± 0.0017 0.0170 ± 0.0016

4.27 ± 0.09 4.40 ± 0.10

63.5 ± 1.8 69.7 ± 1.7

1.02 ± 0.05 0.85 ± 0.04

Calcareous

Control (8) Deadwood (8)

74.7 ± 6.4 80.3 ± 3.1

12.82 ± 0.42 13.02 ± 0.56

489 ± 32 489 ± 52

0.0079 ± 0.0005 0.0083 ± 0.0006

6.65 ± 0.29 6.73 ± 0.27

74.5 ± 1.9 70.5 ± 1.4

0.69 ± 0.05 0.81 ± 0.04

Silicate

Control (23) Deadwood (23)

57.9 ± 6.1 57.6 ± 7.6

16.65 ± 0.33 17.32 ± 0.37

277 ± 25 315 ± 17

0.0129 ± 0.0014 0.0140 ± 0.0013

4.49 ± 0.10 4.61 ± 0.10

64.7 ± 1.6 69.9 ± 1.5

0.98 ± 0.04 0.86 ± 0.04

DC 2

Control (8) Deadwood (8)

57.3 ± 9.1 50.9 ± 8.7

15.93 ± 0.85 15.57 ± 1.07

347 ± 32 316 ± 41

0.0134 ± 0.0280 0.0140 ± 0.0024

4.80 ± 0.44 5.90 ± 0.45

63.4 ± 3.8 67.0 ± 2.3

1.01 ± 0.10 0.91 ± 0.06

DC 3

Control (14) Deadwood (14)

60.2 ± 5.5 56.5 ± 5.4

15.01 ± 0.60 15.89 ± 0.71

359 ± 34 380 ± 32

0.0100 ± 0.0012 0.0107 ± 0.0014

5.56 ± 0.30 5.57 ± 0.30

69.4 ± 1.9 72.5 ± 1.6

0.85 ± 0.06 0.79 ± 0.05

DC 4

Control (8) Deadwood (8)

66.6 ± 14.8 79.4 ± 17.0

15.94 ± 0.55 16.84 ± 0.43

292 ± 58 353 ± 54

0.0125 ± 0.0024 0.0140 ± 0.0025

4.47 ± 0.22 4.69 ± 0.22

66.7 ± 2.1 67.4 ± 1.8

0.91 ± 0.06 0.92 ± 0.05

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Fig. 3. Mean relative differences (indexed to control points, Eq. (2)) in soil properties and density fractions (mg g−1) by forest floor type (level of bioturbation, a), bedrock type (b) and decay class (c). Δ % of all properties except C/N, aromaticity (SUVA280 ) and porosity is based on concentrations. Asterisks indicate significant differences between deadwood and control points (LME), and letters indicate significant differences between independent classes (Wilcoxon or Kruskal-Wallis). Error bars represent one standard error of the mean difference.

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Fig. 4. Conceptual SOM dynamics influenced by deadwood and bedrock. Fragmented wood as well as root and fungal litter (middle) enters the free particulate organic matter (POM) pool. That OM is partially or fully respired along with additional SOM by primed biological growth depending on nutrient availability and climate, which results in more free POM on silicate bedrock and less free POM on calcareous bedrock. With time and decay, transformed wood, root and fungal litter stabilizes as POM occluded within aggregates (right) and mineral-bound OC either freshly adsorbed or replenished by dissolved and microbial OM.

noticeably occur for all deadwood points, yet deadwood with advanced decay did have significant increased oLF-OC concentrations and, at the same time, total SOC stocks compared to control points. In comparison, less decomposed deadwood did not induce any changes in the SOM pools. Together these results affirm hypothesis 2(b). These increases in intermediate stable SOM pools would be the result of several factors, one of which is related to deadwood-fLF dynamics proposed above. First, the continued influx of nitrogen-poor residues and nutrients due to extensive decomposition of deadwood would have prompted enough fungal and root growth to form aggregates. Specifically wooddecaying fungi can extend their mycelia into the organic layer and mineral soil (Cairney, 2005), thus contributing to aggregate formation and an associated increase in oLF-OC concentrations. White-rot in particular, which is often associated with European beech and existed in every sampled log, could play a role too as extra-cellular mucilage of white-rot fungi is rich in polysaccharides (Eriksson et al., 1990), which are important gluing agents for aggregates (Tisdall and Oades, 1982; Caesar-Tonthat, 2002). Additionally, fungal growth directly within soil in response N-poor organic matter has been demonstrated to improve aggregation and aggregate stability (Tisdall and Oades, 1982; Miller and Jastrow, 1990; Bossuyt et al., 2001; Abiven et al., 2009; Lucas et al., 2014). Furthermore, a higher soil occupation by fine roots may also have contributed to increased oLF-OC concentrations through both direct aggregate building and indirect mycorrhizal fungal associations (Daynes et al., 2013). Second, increased DOC input as indicated by elevated WEOC concentrations would have enhanced microbial activity, induced greater microbial biomass (Kappes et al., 2007; Gonzalez-Polo et al., 2013), increased inter-particle bonding and consequently formed aggregates, thus improving oLF-OC concentrations. However, deadwood oLF-OC concentrations were not correlated with WEOC concentrations or any other measured soil properties save stem diameter. Still, increased WEOC and aromaticity at advanced decayed deadwood points relative to control points indicate a change in the composition of SOM. This input of dissolved compounds—and specifically phenolic matter—is related to the type and extent of decay and would have been accompanied by other nutrients (Kuehne et al., 2008; Kahl et al., 2012; Stutz et al., 2017).

at deadwood points on those sites were found, seemingly contradicting our hypothesis. Instead, fLF-OC and WEOC concentrations unexpectedly increased at deadwood points on soils with less bioturbation, i.e., sites with moder forest floor types or on silicate bedrock, which would have been limited by lower soil pH and less nutrients. Despite these seeming contradictions, our results for fLF would be the result of two processes both involving biological mechanisms. First, larger populations of meso- and macrofauna resulting from the presence of deadwood even on sites with characteristically low bioturbation would have vertically transported particulate organic matter into mineral soil (Fig. 4). Deadwood is known to enhance conditions for soil biota beneath and next to downed deadwood logs on acidic forest soils through improved micro-climatic effects, increased nutrient availability and the resulting cascading effects within biological networks (Jabin et al., 2004; Kappes et al., 2006, 2007; Stutz et al., 2017); evidence of improved base saturation for the same samples was reported in Stutz and Lang (2017). Similarly, meso- and macrofaunal bioturbation at sites on calcareous bedrock would have transported particulate matter from deadwood into mineral soil and thus affected the two light fractions. Yet deadwood-stimulated C uptake and respiration would not have been as stoichiometrically limited on nutrientrich calcareous sites compared to nutrient-limited silicate sites, meaning more labile C in the fLF pool would have been mineralized at nutrient-rich sites. Such priming may have even occurred before particulate or dissolved C from deadwood was translocated into underlying soil. Also, other limiting factors for microbial growth such as water would then take precedent if labile OM and nutrients are plentiful. For example, the inverse correlation between Δ fLF and MAP for calcareous sites implies that water limited the primed mineralization of free POM. Second, increased rooting in response to improved nutrient and water availability would have produced more root litter and consequently more particulate organic matter (Fig. 4). Aggregate formation around roots would have also been expected, resulting in oLF instead of fLF, but a combination of fauna and fungal activity along with the coarse texture of the soils on silicate bedrock would have resulted in aggregate disruption as well as aggregate formation. That porosity also increased for deadwood points at silicate sites indicate soil structural changes occurred congruently with the increase in fLF through a dynamic combination of fauna, roots and fungi in response to deadwood. Additionally, improved fungal and root growth may have formed macroaggregates first, whereupon further decomposition of SOM within macroaggregates can create microaggregates more resistant to water slaking and biological disruption (Beare et al., 1994; Gale et al., 2000; Six et al., 2000).

Heavy fraction Dissolved carbon and aromatic compounds are favorable species of organic matter for enhanced chemical stabilization on mineral surfaces specifically through greater microbial biomass and preferential adsorption of phenolic matter (Dungait et al., 2012; Kramer et al., 2012; Cotrufo et al., 2013). For instance, Kallenbach et al. (2016) found the most accumulated C in model soils treated with syringol (a lignin monomer associated with angiosperms) which was related to greater

Occluded light fraction Occlusion of POM within macro- or microaggregates did not 206

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forests were recently estimated to average 61.8 ± 3.7 Mg ha−1 (Grüneberg et al., 2014). If this additional, partially stable OC can be incorporated into forest and soil C models, our estimates of C sequestration within forest soils and life cycle assessments of forest products could be improved (Magnússon et al., 2016). Specifically including the physical accessibility of SOM near deadwood can further distinguish woody litter from leaf litter, which would result in more realistic litter and forest OC stock estimates (Brovkin et al., 2012). And despite these increases in topsoil and possibly subsoil SOC stocks being diminutive in comparison to potential substitution effects of woody biomass in reducing atmospheric CO2 concentrations (Eriksson et al., 2007), maintaining standing biomass and deadwood as recommended to enhance biodiversity can mitigate other climate change-induced disturbances to forest services such as nitrate seepage (Fleck et al., 2017). Our results also indicate that deadwood’s imprint on soil greatly depends on site and decomposition conditions. For instance, nutrient poor and acidic soils (from silicate bedrock) with limited bioturbation are favorable sites for deadwood-induced SOM stabilization and consequently long-term SOC storage. Yet the initial stages of accumulating and stabilizing SOM consist of free POM, i.e., the labile fLF pool. Without considering temporal dimensions of the fLF transferring into oLF and subsequently HF, management activities are susceptible to disturbing those stabilizing processes (Bremer et al., 1994; Grüneberg et al., 2013). Such SOM dynamics near deadwood are likewise essential components to conceptualizing deadwood as “pedogenic hot-spots” for soil development and functioning as defined in Stutz and Lang (2017). Hence, management decisions on removing or retaining deadwood ought to consider ecological conditions and the corresponding consequences for soil and forest services. When also combined with other deadwood management objectives such as improving biodiversity, synergistic benefits to forest health and functioning could be achieved. As outlined in Stutz and Lang (2017) though, pertinent questions remain to be answered concerning the temporal and spatial dimensions of deadwood’s impact on SOM stability, biogeochemical processes and soil development.

abundance of fungi within that treatment. However, no increases in HFOC concentrations were found in our study. Possible explanations include adsorption of “new” OM entering the soil as replacement for previously adsorbed OM mineralized by primed biological activity (Kahl et al., 2012), or, more likely, a saturation of chemically stabilized OM in the Ah horizon and thereby a lack of binding places (Guggenberger and Kaiser, 2003; Schrumpf et al., 2013). If the latter, a stabilization of C in deeper soil horizons is possible as conditions for OM adsorption are favorable there due to low SOM concentrations (Guggenberger and Kaiser, 2003), meaning DOC from deadwood has the potential to contribute to long-term stabilization of OM in subsoils; this, however, was not tested in this study. Alternatively, as SOM in the intermediate pool (oLF) is slowly transfered to the stable pool (HF) according to the conceptual model by Golchin et al. (1997), the time between initiation of deadwood decomposition and our sampling was insufficient to see any effect in the HF pool. Consequences and limitations Our results suggest an influx of organic matter and nutrients prompts a fungal, rooting and fauna response that can result in more fLF through deadwood and root detritus depending on stochiometric and climatic limits to SOM mineralization, more oLF through fungal and root-driven aggregate formation, and eventually more HF. Such deadwood-specific and ecological-related processes indicate deadwood can alter and improve the stability of SOM, partially affirming both our hypotheses. Our methodology, however, limits the certainty to which we can say these processes occurred. For one, the identity of the source of additional C in SOM stocks for any stability pool is unknown. Altered bulk soil C/N ratios as well as WEOC concentrations and aromaticity indicate the compositional quality of SOM changed as a result of deadwood, yet without isotopic or molecular markers to link the altered SOM quantity and quality to deadwood, we cannot rule out redistributed C from roots or fungi as the increase in SOM stocks. Likewise, with a single sonication at 400 J ml−1, all aggregates were assumed to be disrupted simultaneously, meaning oLF in macro- and microaggregates cannot be separated or quantified. Consequently any preferential occlusion of organic matter from deadwood in aggregates of differing size and resulting differences in SOM stability is conjectural. In broader terms though, our results suggest roots and fungal hyphae play a crucial role in SOM stabilization near deadwood through nutrient acquisition and aggregate formation—i.e., biogeochemical and -physical processes that also affect soil functioning as posited by Stutz and Lang (2017). Additionally, eroded litter, moisture and SOM may be caught at deadwood-formed hollows on slopes and consequently sequester C (Berhe et al., 2008). That process and deeper sequestration of OC were not addressed in this study due to exclusion of subsoil and the orientation of sampled deadwood, yet both must be considered if the ecological dynamics of SOM stabilization induced by deadwood are to be understood. Until then, our findings on deadwood effects are minimum values for consideration by forest managers.

Conclusions To conclude, European beech deadwood can contribute to SOM stabilization and OC sequestration in forest topsoils. Our results indicate that processes related to the input of organic matter and the associated soil biological response contribute to the formation of soil ecological hotspots close to deadwood that differ in rates of both C stabilization and nutrient cycling compared to those of normal leaf litter, especially under acidic conditions. As such, managing deadwood to sequester SOC is possible with the amount and its residency time depending on stimulated soil biological activity, nutrient availability and the extent of decomposition. If incorporated into deadwood management strategies, more intact soil and forest ecosystems could be achieved providing sustained or even enhanced ecological services. However, several questions concerning those factors remain unresolved. Stability of SOM under species other than European beech with alternate decay processes may differ. Cascading factors such as fungal growth, plant rooting and fauna trophic networks also remain to be precisely mapped. Furthermore, the temporal and spatial—annual, decadal, vertical and horizontal—extent that SOM stability is altered by deadwood would need to be investigated to fully update soil OC models for forest C accounting. Still, our results demonstrate that deadwood alters SOM stability and therefore long-term forest SOC sequestration in addition to soil and forest ecosystem functioning.

Implications for management Despite these limitations, our results indicate that Fagus sylvatica deadwood increases concentrations of free and aggregate-occluded POM as well as total SOC stocks under certain conditions, and thus affects SOM stabilization and can sequester OC in forest topsoils. At a stand scale, assuming deadwood covers 5% of the surface area, total SOC stocks could increase by 0.64 Mg ha−1 in the top 10 cm2; if deadwood covered 10% of the stand, 1.28 Mg ha−1 would be added. As a comparison, the C stocks of the top 30 cm of mineral soils in German 2

Author contributions K.P.S. and F.L. conceived and designed the study; J.W. and K.P.S. collected field samples, performed the laboratory trials, analyzed the data and wrote the paper; all authors developed and revised the paper.

79.4–66.6 Mg ha −1 = 12.8·0.05 [(100% deadwood cover - 0% deadwood cover) · 5%].

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Acknowledgments We sincerely thank Markus Graf-Rosenfellner, Nicole Specht, Petra Grossmann, Petra Wiedemer and Christine Petschke for their technical expertise; Paula Vollmer and Daniel Dann for their assistance during field work; Helmer Schack-Kirchner for his constructive suggestions; and the two anonymous reviewers for their beneficial comments. We also thank the Forstliche Versuchs- und Forschungsanstalt BadenWürttemberg for providing access to the study sites Conventwald, Siebter Fuß and Schachen; the Forschungsanstalt für Waldökologie und Forstwirtschaft for their support in selecting and for providing access to the forest reserve Wartenberg; and ForstBW and Landesforsten RLP for their help in selecting the remaining study sites. This work was supported by a grant from the Ministry of Science, Research and the Arts of Baden-Württemberg (Az: 33-7533-10-5/81) to Kenton Stutz and Friederike Lang. References Abiven, S., Menasseri, S., Chenu, C., 2009. 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