ISSN 10674136, Russian Journal of Ecology, 2015, Vol. 46, No. 3, pp. 246–251. © Pleiades Publishing, Ltd., 2015.
Carbon, Nitrogen and Phosphorus Stocks in Soil Organic Layer as Affected by Forest Gaps in the Alpine Forest of the Eastern Tibet Plateau1 Q. Wua, b, F. Wua, B. Tana, W. Yanga, X. Nia, and Y. Yanga a
Longterm Research Station of Alpine Forest Ecosystem, Key Laboratory of Ecological Forestry Engineering, Institute of Ecology and Forestry, Sichuan Agricultural University, Chengdu, 611130 China bEcological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang, 621000 China email:
[email protected];
[email protected] Received October 26, 2014
Abstract—Carbon (C) and nutrients storages in soil organic layer play an important role in forest productivity in the alpinegorge area. However, forest gaps during forest regeneration could regulate carbon and nutrients stocks in soil organic layer by controlling hydrothermal environment conditions, but little information has been available on it. Therefore, concentrations and stocks of carbon, nitrogen (N) and phosphorus (P) in fresh litter layer (LL), fragmented litter layer (FL) and humified litter layer (HL) were investigated from gap center, canopy gap and expanded gap to closed canopy in an alpine forest of eastern Tibetan Plateau in later fall (October, 2013). The results showed that the forest gaps reduced the thicknesses of LL and FL, but increased the thickness of HL. Carbon concentrations in LL and FL decreased as affected by forest gaps, whereas both N and P concentrations increased regardless of soil organic layers. Moreover, forest gaps reduced C, N and P stocks in LL and FL, although which in HL increased. In addition, C, N and P stocks were significantly related to negative accumulated temperature regardless of soil organic layers. These results suggest that forest gap could promote carbon and nutrient releases from fresh litters, but limit carbon and nutrients output from humified litters in these alpine forests. Keywords: soil organic layer, forest gap, alpinegorge area, carbon stock, nutrient stocks DOI: 10.1134/S1067413615030091 1
In alpinegorge area, forest ecosystem has a thick organic layer and thin mineral soil layer due to the slow decomposition of plant debris and organic matter accumulation as affected by low temperature, and retarded soil development disturbed by frequent mountain disasters (Li et al., 2012). Consequently, soil organic layer acts as important pools of carbon and nutrients, and plays an important role in forest pro ductivity (Liu et al., 2011, Carvalhais et al., 2014). Meanwhile, soil organic layer is one of the most sensi tive interface to environmental change in the high frigid forest ecosystem (Eglin et al., 2010; Fan et la., 2013; Xu et al., 2014). Forest gap formed by tree fall or other climatic disturbances, is a main form of forest regenerations, which can redistribute the precipita tion, light, organic materials, and other biotic and abi otic factors inside and outside of forest gap, and in turn control the decomposition and accumulation of organic materials on the forest floor (Millar et al., 2007), i.e. the concentrations and stocks of carbon and nutrients in soil organic layer inside and outside of for 1 The article is published in the original.
est gap. However, there is still lack of understanding the links of forest gap to the concentrations and stocks of carbon and nutrients in soil organic layer. Recent studies have demonstrated that forest gap can substantially redistribute ambient microclimate conditions (Zhang and Zak, 1995; Ritter et al., 2005; Sariyildiz, 2008) and alter the chemical traits of litter (Prescott et al., 2003; Scharenbroch and Bockheim, 2008). In winter, thick snow cover in opened forest gaps acting a positive insulator for maintaining suffi cient warm temperatures, which could support a rea sonable level of biotic activity underneath the snow pack (Campbell et al., 2005; Streit et al., 2014) and enhance the stoichiometric changes in material traits (Saccone et al., 2013). Consequently, labile compo nents are quickly released from the foliar litter incu bated under deep snow cover in forest gaps compared with in closed canopy (Baptist et al., 2010; Bokhorst et al., 2013). Furthermore, the higher precipitation in forest gaps resulting in a stronger hydrological leach ing can give a great contribution to nutrient loss in growing season (Elliott, 2013). Accordingly, forest gap could regulate organic matter decomposition, subse
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To test the hypothesis, we conducted a field inves tigation on soil organic layers containing fresh litter layer (LL), fragmented litter layer (FL) and humified litter layer (HL) from gap center, canopy gap and expanded gap to closed canopy in an alpine forest of the east Tibetan Plateau. The forests play important regulatory roles in the regional climate and water con servation. However, soil formation and development is limited by extremely low temperatures, frequent geo logical disasters and inefficient ecosystem productivity (Yang et al., 2005). N and P are known as the primary limited nutrients in ecosystem productivity. Hence, the role of soil organic layer in controlling carbon and nutrients fluxing from plant to soil is crucial for soil pool in this alpine forest ecosystem. Our previous studies have demonstrated that forest gap significantly affects the process of foliar litter decomposition and humification (He et al., 2013; Ni et al., 2014). How ever, information on the feedback of carbon and nutri ents storages in soil organic layer to forest gaps is scarce. Therefore, the objective was to interpret car bon and nutrients storages feedback to uninterrupted natural forest regeneration. MATERIALS AND METHODS Site Description This study was conducted in the Miyaluo Nature Reserve (31°14′–31°19′ N, 102°53′–102°57′ E, alti tude 2458–4619 m), Sichuan Province of China. This reserve is a transitional zone between the Tibetan Pla teau and the Sichuan Basin (Yang et al., 2005). The annual mean temperature at the sampling sites is 2.7°C, with mean temperatures of –8.7°C and 9.5°C being observed in January and July, respectively. The annual mean precipitation is 850 mm. The winter gen erally extends from late October to late April of the fol lowing year, showing a maximum snow depth of approximately 50 cm in the center of forest gaps and a freezethaw cycle duration of approximately 120 days (Wu et al., 2010). The seasonal snow cover begins from November to April of the following year (Tan et al., 2011). The experimental sites are dominated by fir (Abies faxoniana) in the forest canopy. The thin soil is classified as dark brown soil (Yang et al., 2005). The canopy gaps and expanded gaps presently from the sampling sites cover 23.05% and 12.60%, respectively (Wu et al., 2013). RUSSIAN JOURNAL OF ECOLOGY
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Gap center
10 0 –10 Daily mean temperature, °C
quently changing the storage of C and nutrients. How ever, little attention has been paid to the effects of for est gap on C and nutrients storage in the high frigid forest, which greatly limited our understanding in the processes of forest regeneration. Therefore, we hypothesized that forest gaps in the alpine forest can reduce the storages of carbon, nitrogen and phospho rus in soil organic layer.
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Canopy gap
10 0 –10 20
Expanded gap
10 0 –10 20
Closed canopy
10 0 –10 0 10 0 11 0 12 01 3 26, 2 26, 2 26, 2 26 , 2 . . . . t t t t c c c c O O O O Date Fig. 1. Daily mean temperatures in the gap center, canopy gap, expanded gap and the closed canopy from Oct. 26, 2010 to Oct. 26, 2013.
Experimental Design Following the method of Wu et al. (2013), we estab lished three replicate sampling sites of 25 m × 25 m in size, at least 500 m apart, in three similar 130yearold dominant fir forest stands (31°14′ N, 102°53′ E, alti tude 3579–3582 m) which shows homogeneous aspects, slopes and gap formation patterns and dura tions. Furthermore, we also manipulated four plots measuring 1 m × 1 m in size, located in four directions (north, east, south and west), in gap center, canopy gap, expanded gap (Schliemann and Bockheim, 2011) and the closed canopy, separately, at each site for sam pling. We measured the thicknesses of the samples in soil organic layers containing fresh litter layer (LL), fragmented litter layer (FL) and humified litter layer (HL) in the 12 plots of each forest gap and the closed canopy using a ruler. The samples were corrected on 26 October in 2013 when the growing season is dor mant with temperature down to zero. To quantitatively clarify the environmental factors associated with the various gaps, we measured the snow depth on the sampling site and the temperature from Oct. 26, 2010 to Oct. 26, 2013 in our longterm experiment (see Table 1; Fig. 1). Snow depths were measured using a ruler at the four plots under the three gap classes and the closed canopy at each site. The temperatures above ground under the three gap classes and the closed canopy were obtained every two hours using iButton automatic recorders (iButton DS1923F5, 2015
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(PD, the days of the temperature above °C) and nega tive days (ND, the days of the temperature below °C) (Table 1).
(a) GC
CG
EG
CC
c c
LL
b
Sample Analyses
a
The filed samples were sieved (2 mm) to remove stones and macrofauna. The subsamples were oven dried at 70°C for 48 h, and the remaining masses were weighed to determine the moisture contents (Fig. 2b). We then used them to determine the contents of car bon, nitrogen and phosphorus following the dichro mate oxidation, Kjeldahl and phosphomolybdenum yellow spectrophotometry methods (Lu, 1999).
c c
FL
b a
Soil organic layer
a
HL
a
a
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4 6 8 Thickness, cm (b)
2
10
Statistical Analyses and Calculation
a
LL
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a
Twoway ANOVA with Tukey’s HSD was per formed to test the effects of the soil organic layers, for est gaps and their interactions on the storages of car bon, nitrogen and phosphorus. Oneway ANOVA was employed to test for significant differences in snow depths, temperature parameters, thicknesses, mois ture contents, the contents and storages of carbon, nitrogen and phosphorus between the forest gaps and the closed canopy. A stepwise regression analysis was conducted to test the effects of dominant factors on the storages of carbon, nitrogen and phosphorus. The above analyses were performed using SPSS 20.0 (IBM SPSS Statistics Inc., Chicago, IL, USA).
a a
FL
b
a
a b a
HL
ab
c
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2
4 6 8 Moisture content, %
10
Fig. 2. The (a) thicknesses and (b) moisture contents of fresh litter layer (LL), fragmented litter layer (FL) and humified layer (HL) in the three forest gaps and the closed canopy. GC: gap center, CG: canopy gap, EG: expanded gap, CC: closed canopy. The presented values are the means of n = 12 observations, with error bars representing standard deviations. Different lowercase letters denote sig nificant (P < 0.05) differences between the forest gaps and the closed canopy.
RESULTS The Thicknesses and Moisture Contents of Soil Organic Layer
Maxim/Dallas Semiconductor, Sunnyvale, CA, USA). In addition, to represent the temperature parameters of the three forest gap classes and the closed canopy, we used the recorded data to calculated the following values: daily mean temperature (DMT; Fig. 1), posi tive accumulated temperature (PAT, sum of tempera tures above °C), negative accumulated temperature (NAT, sum of temperatures below 0°C), positive days
The thicknesses of soil organic layers were increased with the increase of soil profile in the gap center, but an inverse pattern in the closed canopy (Fig. 2a). However, the thicknesses of LL and FL in forest gaps were thinner than that in the closed canopy (Tukey’s HSD, P < 0.05; closed canopy > expanded gap > canopy gap (gap center)). In contrast, the thick ness of HL showed an opposite pattern. Moreover, the moisture contents of LL, FL and HL varied with soil profile. The expanded gap exhibited the lowest mois
Table 1. Snow depth (SD), daily mean temperature (DMT), positive accumulated temperature (PAT), negative accumu lated temperature (NAT), positive days (PD) and negative days (ND) in the three forest gaps and the closed canopy accord ing to three years dynamic investigation. The presented values are the means of n = 3 observations. Different lowercase let ters denote significant (P < 0.05) differences between the forest gaps and the closed canopy Gaps Gap center Canopy gap Expanded gap Closed canopy
SD
DMT
PAT
NAT
PD
ND
46.80 ± 2.30 a 29.40 ± 3.44 b 21.40 ± 2.50 c 0.78 ± 0.67 d
5.02 ± 0.41 a 3.96 ± 0.61 ab 3.06 ± 0.28 b 3.59 ± 0.60 b
2046 ± 146 a 1696 ± 220 ab 1434 ± 100 b 1632 ± 219 ab
–213 ± 9 a –248 ± 10 b –316 ± 10 c –319 ± 10 c
267 ± 5 a 245 ± 6 b 248 ± 6 b 237 ± 7 b
98 ± 5 160 ± 6 117 ± 6 128 ± 7
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(a) LL FL Soil organic layer
HL
c b c
a
b b
b c d c
b
c
d
b
c b
a
0 50 100 Nitrogen content, g kg–1
a a a
LL
HL
d
a b a a
Gap center Canopy gap Expanded gap Closed canopy
a
a FL ba a
HL
b
c
a
a
HL
0 0.5 1.0 1.5
45 ×103 Carbon storage, t ha–1
a ba a b
HL
0
a a
b
c
0.2
0.4 1.0 1.5 ×103 Nitrogen storage, t ha–1
(c)
d LL cb
FL
(b)
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bb a a
FL
a
HL
0 200 400 Carbon content, g kg–1 (c)
FL
c
FL
a a
b
LL
(a)
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b a b
Soil organic layer
b a a
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c
d
b
a
Gap center Canopy gap Expanded gap Closed canopy
0 5 10 30 40 Phosphorous storage, t ha–1
0 1 2 Phosphorous content, g kg–1 Fig. 3. The contents of (a) carbon, (b) nitrogen and (c) phosphorus in fresh litter layer (LL), fragmented litter layer (FL) and humified layer (HL) in the gap center, can opy gap, expanded gap and the closed canopy. The pre sented values are the means of n = 12 observations, with error bars representing standard deviations. Different low ercase letters denote significant (P < 0.05) differences between the forest gaps and the closed canopy.
Fig. 4. The storages of (a) carbon, (b) nitrogen and (c) phosphorus in fresh litter layer (LL), fragmented litter layer (FL) and humified layer (HL) in the gap center, can opy gap, expanded gap and the closed canopy. The pre sented values are the means of n = 12 observations, with error bars representing standard deviations. Different low ercase letters denote significant (P < 0.05) differences between the forest gaps and the closed canopy.
ture content of FL while the closed canopy showed the lowest value of HL (Fig. 2b).
The Stoichiometric Characters of C, N and P
The contents of C, N and P The carbon contents of LL and FL were signifi cantly (P < 0.05) lower in forest gaps compared with that in the closed canopy, whereas an opposite result was observed for the value of HL (Fig. 3a). However, both nitrogen (Fig. 3b) and phosphorus contents (Fig. 3c) of LL, FL and HL were significantly (P < 0.05) higher in the forest gaps compared to in the closed canopy. The storages of C, N and P The forest gaps affected the storages of carbon (F3.11 = 251.4, P < 0.001), nitrogen (F3.11 = 353.8, P < 0.001) and phosphorus (F3.11 = 223.0, P < 0.001), with a high variation among soil organic layers (P < 0.001 of twoway ANOVA, Table 2). The carbon, nitrogen and phosphorus storages of LL were lower in forest gaps than that in closed canopy, whereas the values of HL were lower in the closed canopy than that in canopy gap and expanded gap (Figs. 3a–3c). In addition, stepwise regression analyses revealed that carbon, nitrogen and phosphorus storages in the three layers were significantly related to negative accumulated temperature (Table 3). RUSSIAN JOURNAL OF ECOLOGY
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Both the C : N and C : P ratios of LL and FL, as well the N : P ratio of FL was significantly higher in the closed canopy relative to the forest gaps (Fig. 5). How ever, the highest N : P ratios of LL and HL, and the C : P ratio of HL was obtained in canopy gap. DISCUSION Our results here suggested that forest gaps greatly reduced the storages of carbon, nitrogen and phos phorus of LL and FL, but increased the storages of HL, which partially verified the hypothesis that carbon and nutrients storages in soil organic layer would be reduced by forest gaps. The results also implied that more carbon and nutrients would be released from fresh litter in forest gaps, but the carbon, nitrogen and phosphorus in humified litters could be accumulated in mature organic matter. Table 2. F values for twoway ANOVA with Tukey’s HSD testing for carbon (C), nitrogen (N) and phosphorus (P) storage for the effects of the layers, forest gaps and their combined interactions
Factors
df
C
N
P
Layer Gap Layer × Gap
2 3 6
251.4** 16.9** 21.2**
353.8** 638.0** 178.9**
223.0** 902.6** 65.9**
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Table 3. Determination coefficients (R2) and step number, in parentheses, for stepwise regression analyses of carbon (C), nitrogen (N) and phosphorus (P) storage, affected by environmental factors C
Step number 1 2 3
N
P
LL
FL
HL
LL
FL
HL
LL
FL
HL
NAT (0.915) ND (0.967) DMT (0.983)
NAT (0.649) ND (0.964)
NAT (0.797) PD (0.872)
NAT (0.949)
NAT (0.880)
NAT (0.924)
NAT (0.887) ND (0.986)
ND (0.340) NAT (0.784)
NAT (0.897)
DMT: daily mean temperature, NAT: negative accumulated temperature, PD: positive days, ND: negative days.
Forest gap is open without standing trees compared to the closed canopy, so plant litters fall less in forest gaps with thinner thickness of fresh litter (Fig. 2a). However, recent evidences demonstrated that forest gap could reestablish the environment conditions and then constrain the decay of fresh litter (Zhang and Liang, 1995; Zhang and Zak, 1995; Sariyildiz, 2008). Carbon and nutrients could be released less from fresh litter, showing high concentrations in forest gaps (Figs. 3b, 3c). Here, high concentrations of carbon were obtained in fresh and fragmented litter, implying that the carbon release of fresh materials was pro moted by forest gaps. While in the humified layer, the releases of carbon, nitrogen and phosphorus showed the same pattern that forest gap reduced the releases of carbon and nutrients. These suggested that with the increase of soil profile, the decay of organic matter and nutrients could be not sensitive to forest gaps. (a) b
LL
Soil organic layer
c
FL
b
HL
b a a a
0
LL FL HL
a
(b)
bb
bb
LL
a
b b b
FL
a
c
HL
4 8 12 C : N ratio (c) b a c b b d c a b a bb
0
b
a a
a bb
200 400 C : P ratio
600
Gap center Canopy gap Expanded gap Closed canopy
0 10 20 30 40 50 60 N : P ratio Fig. 5. The ratios of (a) carbon to nitrogen, (b) carbon to phosphorus and (c) nitrogen to phosphorus in fresh litter layer (LL), fragmented litter layer (FL) and humified layer (HL) in the forest gaps and the closed canopy. Different lowercase letters denote significant (P < 0.05) differences between the forest gaps and the closed canopy.
In forest gaps, the storages of carbon, nitrogen and phosphorus were decreased both in fresh and frag mented layer, but be promoted in humified layer, which stored large amount of carbon and nutrients compared to the more fresh layers (Fig. 4). This differ ence could be contributed to the balance between the input and the output of litter materials. On one hand, little litter fall presented in forest gaps (Fig. 2a), with less fluxes of carbon and nutrients. On the other hand, fresh litter would be decomposed more in forest gaps. The deep insulating of snow cover (Baptist et al., 2010; Bokhorst et al., 2013) and the stronger hydraulic leaching (Elliott, 2013) in winter, as well the greater photodegradation of solar radiation (Austin and Viv anco, 2006) could highly contributed to the releases of carbon and nutrients during decay. The results of repeated measures ANOVA indicated that the storages of carbon, nitrogen and phosphorus of LL, FL and HL were related to negative accumulated temperature, showing that negative temperature in winter is critical for the decay of litter material in this alpine forest. In conclusion, the storages of carbon, nitrogen and phosphorus of LL and FL were constrained, but stim ulated for HL in forest gaps. However, both the stor ages of carbon and nutrients in various organic layers were related to negative accumulated temperature. These results suggesting that the decomposition of carbon and nutrients of fresh litters could be stimu lated by forest gap, but the humified matters could be constrained in the process of forest regeneration in alpine forest. ACKNOWLEDGMENTS This study was financially supported by the National Natural Science Foundation of China (31270498, 31170423), the National Key Technolo gies R and D Program of China (2011BAC09B05), the Postdoctoral Foundation of China (2012T50782) and the Sichuan Youth Science and Technology Foun dation (2012JQ0008, 2012JQ0059).
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