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Stand age and species traits alter the effects of understory removal on litter decomposition and nutrient dynamics in subtropical Eucalyptus plantations
Global Ecology and Conservation 20 (2019) e00693
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Global Ecology and Conservation journal homepage: http://www.elsevier.com/locate/gecco
Original Research Article
Stand age and species traits alter the effects of understory removal on litter decomposition and nutrient dynamics in subtropical Eucalyptus plantations Yuanqi Chen a, b, e, Yanju Zhang b, c, Jianbo Cao b, c, Shenglei Fu d, Shuijin Hu e, Jianping Wu f, Jie Zhao g, Zhanfeng Liu b, * a
Hunan Province Key Laboratory of Coal Resources Clean-utilization and Mine Environment Protection, Hunan University of Science and Technology, Xiangtan, 411201, China Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China c University of Chinese Academy of Sciences, Beijing, 100049, China d College of Environment and Planning, Henan University, Kaifeng, 475004, China e Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695, United States f School of Ecology and Environmental Science, Yunnan University, Kunming, 650091, China g Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 April 2019 Received in revised form 21 June 2019 Accepted 21 June 2019
Litter decomposition is a crucial ecological process that regulates nutrient cycling. However, the effects of understory plants and overstory trees on litter decomposition and nutrient dynamics are still poorly understood. We conducted understory plants removal and/or overstory trees removal to examine the resulting effects on litter decomposition and nutrient mineralization in two Eucalyptus plantations with contrasting ages (8-yr-old, 29-yr-old) in subtropical China. Litter bags containing naturally senesced leaves of either overstory Eucalyptus urophylla or understory Dicranopteris dichotoma were placed in field and periodically collected for analyses of carbon (C), nitrogen (N), phosphorus (P) and calculation of mass loss. Our results showed that understory plants removal significantly reduced litter decomposition of E. urophylla in both plantations, but N and P mineralization were reduced only in the 8-yr-old plantation. In contrast, it reduced litter decomposition of D. dichotoma only in the 29-yr-old plantation, but had no effects on N and P mineralization in either plantation. In comparison, overstory tree removal did not have any effects on decomposition or mineralization of N and P of E. urophylla and D. dichotoma litters. These results indicate that the role of understory plants in mediating litter decomposition and nutrient mineralization is more important than overstory trees, and it can be altered by stand age and plant species. Our findings could facilitate the understanding of ecological processes of litter decomposition and nutrient mineralization in subtropical forest ecosystems. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords: Leaf litter Understory plant Nutrient mineralization Subtropical forest Stand age Plant identity
* Corresponding author. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, No. 723, Xingke Road, Guangzhou, 510650, China. E-mail address: [email protected] (Z. Liu). https://doi.org/10.1016/j.gecco.2019.e00693 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
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1. Introduction Litter decomposition is a fundamental ecological process that regulates nutrient cycling (Versini et al., 2014; Bravo-Oviedo et al., 2017), and is also a key determinant controlling carbon (C) cycling in forest ecosystems (Creamer et al., 2015). When litter decomposes, the litter-derived C could be incorporated into microbial biomass and/or be respired, simultaneously, the input of litter-derived C could stimulate soil organic C decomposition by altering soil microbial activity and community structure (Cotrufo et al., 2015). In reverse, the soil microbial biomass and microbial community structure could impact litter decomposition (Schneider et al., 2012; Müller et al., 2017). Besides, soil microclimate and litter quality also affect litter decomposition process (Petraglia et al., 2019) and can explain over 31% of the variance in litter decomposition in subtropical plantations (Seidelmann et al., 2016). In subtropical forest ecosystems, understory plants play a critical role in sustaining soil microclimate and driving ecological processes, especially in plantation forests with a large understory plant biomass (Zhao et al., 2012). The understory biomass was above 17 Mg ha1 and contributed 18.7e46.6% of the plant carbon pool in subtropical plantations (Chen et al., 2015; Fan et al., 2015). Wang et al. (2014) found that understory removal significantly reduced soil nitrogen (N) mineralization and nitrification rates in two subtropical lumber plantations. Our previous studies found that understory plants made a significant contribution to soil respiration, soil food web structure, litter decomposition, and net ecosystem productivity in subtropical plantations (Zhao et al., 2012; Wu et al., 2014). However, most studies mainly focused on the tree leaf litters, and few attention has been paid to the leaf litters of understory plant in forest ecosystems (Aponte et al., 2012; Schuster and Dukes, 2014). In China, plantation area of approximately 69 million hectares is one third of that of the world with over 60% of that distributed in subtropics (China Forestry Database; Wang et al., 2010). Eucalyptus plantations is approximately 34% of the total plantation area in southern China, which cover 4.50 million hectares as Eucalyptus trees have high productivity and rapid economic returns (China Forestry Database; China Science Daily, 2015). Understory plant, which was dominated by Dicranopteris, contributed up to 33.9% of the net primary production of the Eucalyptus plantations in southern China (Wu et al., 2014). However, understory removal is still a common practice to prevent fire and eliminate the competition with target tree species in forest management (Campbell et al., 2012; Zhou et al., 2018). To our knowledge, little is known about the litter decomposition process and nutrient dynamics of understory plant in such ecosystem. Moreover, the responses of litter decomposition and nutrient dynamics of understory plant to the removal of overstory trees are not well understood. Forest age also plays an important role in controlling litter decomposition (Skorupa et al., 2015). Microclimate, litter quality and soil microbial community composition will vary with forest age and result in various responses of litter decomposition to disturbance (i.e., understory removal, overstory thinning) consequently (Trap et al., 2013; Wu et al., 2013; Trogisch et al., 2016; Yin et al., 2016). Our previous study also found that understory plants removal altered the fate of soil labile C in the plantations of different ages (Chen et al., 2019). However, there is still knowledge gap about how the loss of understory plants and/or overstory trees respectively impact litter decomposition and nutrient dynamics in forests of different ages (Qiao et al., 2014). In this study, understory removal and/or tree removal were conducted in two Eucalyptus plantations of contrasting stand ages (8- and 29-yr-old). We hypothesized that (1) tree removal and understory removal would retard litter decomposition and nutrient dynamics by changing the composition of soil microbial community and soil microclimate; (2) the effects of tree removal and understory removal on litter decomposition and nutrient dynamics depend on stand age and plant species due to their effects on soil microclimate and litter quality. 2. Materials and methods 2.1. Study site This experiment was carried out at the Heshan National Field Observation and Research Station of Forest Ecosystem (112.83 E, 22.57 N), which is located in Heshan city, Guangdong Province in southern China. The mean altitude is 80 m. The climate in this region is a typical subtropical monsoon climate with a distinct wet and dry season (Chen et al., 2015). The mean annual temperature is 22.3 C, and the mean precipitation is 1688 mm yr1 during 2005e2012. The soil is classified as Ultisol (Chen et al., 2015). The studied Eucalyptus plantations were established on homogenous degraded hilly lands, and Eucalyptus urophylla were planted at a spacing of 3 m 2 m in 2005 and 1984, respectively. In these two plantations, understory plants were highly dominated by Dicranopteris dichotoma. The details of understory plants were reported in Wu et al. (2011). 2.2. Experimental design Experimental plots were established in late winter of 2007 with three replicated plots in both 8- and 29-yr-old plantations (Wu et al., 2011). The nearest distance of plots was more than 100 m away from each other. Tree girdling and understory removal were conducted respectively or jointly in each plantation in 2007. Understory plants were removed by harvesting aboveground parts of plants and the new understory plant growth was removed monthly by hand as some of them can sprout and grow from remnant roots in the subplots with understory removal. Each plot (10 m 10 m) was
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divided into four subplots, which corresponded to four treatments. The details of plots has been described in Wu et al. (2011). This study was conducted in 2013, tree girdling was equivalent to tree removal as the girdled trees died after 1 year of treatment and then removed out of subplots. That is, four treatments in this study included: (1) no tree removal and no understory removal (CK), (2) understory removal only (UR), (3) tree removal only (TR), and (4) understory removal and tree removal (TUR). 2.3. Leaf litter decomposition experiment The fresh leaf litter of Eucalyptus and Dicranopteris was respectively collected from two studied plantations with understory plant and overstory tree on April 2013. Thereafter, all leaf litters of each species from the same plantation were mixed homogeneously and placed into litter bags (20 cm 20 cm) made from polyvinyl screen. To alleviate the effect of mesh size of litter bag on soil biota and insects, the mesh size of one side was 0.5 mm and the other side was 2.0 mm, which was faced up in order to enable access for some soil biota and insects (Melillo et al., 1982). Each bag was filled with 8.0 g (oven-dried weight) leaf litter of Eucalyptus or Dicranopteris. Six litter bags containing the leaf litter of each species were placed on the soil surface in each subplot. In total, 288 litter bags were prepared for decomposition. The decomposition of leaf litter started on 17 May, 2013 and lasted 17 months. Every two bags (one with leaf litter of Eucalyptus, another with leaf litter of Dicranopteris) were retrieved from each subplot firstly on 18 July 2013, and then quarterly on 22 October 2013, 16 January 2014, 21 April 2014, 15 July 2014, and 17 October 2014, respectively. The retrieved litters were cleaned using forceps, dried in an oven at 65 C for 72 h, and then weighted to calculate the percentage of litter mass loss (LML). Decomposition rate of leaf litter was determined by the percentage of litter mass loss. LML (%) ¼ (8.0 - interval weight of litter) 100/8.0, where the 8.0 is the initial weight of litter in each bag. Meanwhile, the C, N and P concentration of retrieved litters were determined by using potassium dichromate oxidation method, Kjeldahl method, and the Mo-Sb colorimetric method, respectively (Bao, 2000). In all subplots, soil temperatures at the 0e5 cm soil layer were recorded by button thermometers (LI-COR Biosciences, Lincoln, NE, USA) from Aug. 2014 to Jun. 2015. 2.4. Soil sampling and analysis At the start of litter decomposition experiment, soil sample (0e20 cm depth) was collected with five cores (3.0 cm inner diameter) and combined into a composite sample for each subplot. In total, 24 samples were collected. The litter on soil surface was removed carefully when soil sample was taken. Soils were thoroughly homogenized by sieving with 2 mm mesh. Visible plant roots, rocks, and soil macrofauna in soils were removed by hand before analysis. Soil organic C (SOC) concentration was determined with the traditional potassium dichromate oxidation method (Bao, 2000). Soil moisture content (SMC %, moisture content per 100 g dry soil) was measured by oven-drying for 24 h at 105 C. N and P concentrations of soil and litter were determined with Kjeldahl method, and sulfuric acid solution and Mo-Sb Antispectrophotometer method, respectively (Bao, 2000). Soil microbial community was characterized by using phospholipid fatty acids (PLFAs) analysis as described by Bossio and Scow (1998). Concentration of each PLFA was calculated based on 19:0 internal standard concentration. PLFAs used as bacterial biomarkers were i15:0, a15:0, i16:0, 18:1u7, i17:0, a17:0, cy17:0, cy19:0; the PLFAs used as fungal biomarkers were 18:1u9c and 18:2u6,9c, and total microbial biomass was considered to be represented by bacterial biomarkers, fungal biomarkers, and other PLFAs such as 16:1u5c, 10 Me 16:0, 10 Me 17:0, 10 Me 18:0 (Frostegård and Bååth, 1996; Bååth and Anderson, 2003; Joergensen and Wichern, 2008). 2.5. Data analysis Nutrient remaining (%) was calculated by dividing remaining and initial nutrient pool. Meanwhile, an exponential decay model was used to analyze the relationship between initial litter remains and decomposition time: X ¼ a*e-kt, where X is the fraction of initial litter remains at time t (yr), a is the simulation parameter, e is the base of natural logarithm, k is the decomposition constant (yr1) over the whole decomposition period. One-way ANOVA was performed to explore the difference in initial properties of leaf litter between the 8- and 29-yr-old plantations, and soil properties among different treatments at the start of litter decomposition experiment in two plantations. T-test was carried out when the data could not meet the requirements of one-way ANOVA. Two-way ANOVA was employed to test the effects of understory removal and tree removal on soil microbial community in the 8- and 29-yr-old plantations. RMANOVA was used to test the effects of understory removal and tree removal on leaf litter decomposition, nutrient dynamics, and soil temperature in two plantations. In addition, the effects of stand age, understory removal and tree removal on soil temperature and soil moisture content were analyzed by three-way ANOVA. The effects of stand age, plant species, understory removal and tree removal on the LML and decomposition constant (k) were tested by four-way ANOVA. Pearson correlation analyses were employed to test the relationships between soil properties (i.e., physicochemical properties and soil microbial communities) and decomposition indices (i.e., the LML and the fraction of litter C, N, and P remaining at the end of experiment) in two studied plantations. All statistical analyses were carried out with SPSS 18 (SPSS, Inc, Chicago, IL) and statistical significance was determined at P < 0.05 level.
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Table 1 Results of two-way ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on total soil microbial biomass (TMB), bacterial biomass (B), fungi biomass (F), fungi: bacteria ratio (F:B) (biomass expressed as PLFAs) in the 0e10 cm soil layer, the concentration of soil organic carbon (SOC) and soil nitrogen (TN), soil C:N ratio, and soil moisture content (SMC) in 0e20 cm soil layer at the start of litter decomposition experiment, and soil temperature (ST) in 0e5 cm soil layer during Aug. 2014 to Jun. 2015 in the 8- and 29-yr-old plantations. 8-yr-old
29-yr-old
UR
TMB B F F:B SOC TN C:N ST SMC
TR
UR*TR
UR
TR
UR*TR
F
P
F
P
F
P
F
P
F
P
F
P
0.21 0.00 3.03 5.08 0.24 0.03 1.34 0.69 0.75
0.661 0.992 0.120 0.054 0.638 0.874 0.280 0.430 0.412
0.66 0.44 0.26 0.00 0.00 0.01 0.10 0.17 0.56
0.442 0.524 0.626 0.961 0.990 0.939 0.765 0.688 0.476
0.00 0.00 0.08 0.39 0.04 0.02 0.02 1.46 0.39
0.999 0.992 0.873 0.550 0.847 0.893 0.886 0.262 0.549
6.31 4.27 17.96 5.08 8.31 3.15 0.68 20.94 8.35
0.036 0.073 0.003 0.054 0.020 0.114 0.434 0.002 0.020
0.29 0.27 0.11 0.37 0.31 1.39 0.27 0.75 0.25
0.605 0.621 0.749 0.560 0.590 0.272 0.617 0.412 0.632
0.27 0.17 0.08 0.53 0.46 0.96 0.03 0.28 1.90
0.615 0.688 0.780 0.489 0.517 0.355 0.875 0.611 0.205
3. Results
3.1. Soil characteristics and initial litter quality 3.1.1. Soil characteristics Understory removal significantly decreased total microbial biomass (TMB) and fungal biomass (F), and decreased the bacterial biomass (B) and F:B ratio to some extent in the 29-yr-old plantation (Table 1). Surprisingly, the significant effects or trends were not observed, except that the F:B ratio showed a decreased trend in the 8-yr-old plantation. Furthermore, tree removal did not show any significant effect on composition of soil microbial community in two studied plantations (Table 1). Understory removal significantly decreased soil C concentration in the 29-yr-old plantation, but not in the 8-yr-old plantation. Soil N and soil C:N ratio were not affected by understory removal and tree removal both in the 8- and 29-yr-old plantations (Table 1). Understory removal significantly increased soil temperature and decreased soil moisture content in the 29-yr-old plantation, but not in the 8-yr-old plantation. Meanwhile, tree removal did not affect them both in the 8- and 29-yr-old plantations (Table 1). Soil temperature in the 8-yr-old plantation was higher than that in the 29-yr-old plantation (P ¼ 0.001). Conversely, soil moisture content was lower in the 8-yr-old plantation than in the 29-yr-old plantation (P < 0.001). The interaction effects of understory removal, tree removal and stand age on soil temperature and soil moisture content were not significant (all P > 0.210). 3.1.2. Initial litter quality The higher litter C concentration and C:P ratio, lower N and P concentration of Eucalyptus than that of Dicranopteris were detected both in the 8- and 29-yr-old plantations (Table 2). In addition, the litter P concentration of Eucalyptus was lower in the 8-yr-old plantation than that in the 29-yr-old plantation (P ¼ 0.010), but there was no significant difference in litter C, N, C:N ratio of Eucalyptus between two plantations (P ¼ 0.051, 0.082, and 0.905, respectively). The litter C, N, and P concentrations of Dicranopteris were lower (P ¼ 0.049, <0.001, and 0.040, respectively), but C:N ratio was higher (P ¼ 0.001) in the 8yr-old plantation than that in the 29-yr-old plantation (Table 2).
Table 2 The initial chemical properties of leaf litter in the 8- and the 29-yr-old plantations (mean ± SE, n ¼ 3). C, N and P (%) are the concentrations of total carbon, nitrogen and phosphorus in the leaf litter; C:N, C:P, and N:P are the ratios of carbon to nitrogen, carbon to phosphorus, and nitrogen to phosphorus concentrations in the leaf litter. Properties
C (%) N (%) P (%) C:N C:P N:P
8-yr-old
P value
E. urophylla
D. dichotoma
51.59 ± 1.10 A 0.73 ± 0.05 A 0.025 ± 0.001 B 70.48 ± 9.95 A 2037 ± 74.4 A 30.03 ± 1.91 A
45.80 ± 0.76 b 0.98 ± 0.02 b 0.037 ± 0.002 b 46.67 ± 1.15 a 1253 ± 76.4 a 26.97 ± 2.36 a
0.020 0.012 0.010 0.248 0.006 0.371
(20.60) (19.47) (21.39) (2.38) (47.66) (1.02)
29-yr-old
P value
E. urophylla
D. dichotoma
55.24 ± 1.16 A 0.92 ± 0.06 A 0.03 ± 0.001 A 60.53 ± 5.65 A 1856 ± 73.5 A 31.02 ± 2.09 A
48.05 ± 0.25 a 1.47 ± 0.03 a 0.048 ± 0.00 a 32.72 ± 0.85 b 994.3 ± 10.9 a 30.40 ± 0.45 a
0.004 0.002 0.000 0.036 0.006 0.789
(36.55) (59.42) (756.3) (4.86) (2.09) (0.08)
P values are from one-way ANOVA of species in the plantation with the same stand age. The different uppercase and lowercase letters mean significant differences between 8- and 29-yr-old plantations for the leaf litter of E. urophylla and D. dichotoma, respectively.
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3.2. Leaf litter decomposition Leaf litter decomposition was represented by the percentage of litter mass loss (LML). Two-way RM ANOVA indicated that understory removal significantly decreased the LML of Eucalyptus in the 8- and 29-yr-old plantation (Fig. 1a and b), and the LML of Dicranopteris in the 29-yr-old plantation (Fig. 1d). However, tree removal did not show significant effects on the LML of Eucalyptus and Dicranopteris in the 8- and 29-yr-old plantations. Four-way RM ANOVA showed that stand age, plant species, and understory removal significant affected the LML (all P < 0.001), yet tree removal did not (P > 0.05). The interaction effect of stand age and understory removal, and the interaction effect of plant species and understory removal on the LML were significant (P ¼ 0.001, and P < 0.001, respectively), but other interaction effects were not significant (all P > 0.116). Understory removal and plant species significantly affected leaf litter decomposition constant (four-way ANOVA, P < 0.001), but stand age and tree removal did not (P > 0.05). Leaf litter decomposition constant was lower when the understory plants was absent (Fig. 1e and f). The interaction effects of understory removal, tree removal, stand age, and plant species on decomposition constant were not significant (P > 0.05). 3.3. Nutrient mineralization Understory removal significantly increased C remaining of Eucalyptus litter both in the 8- and 29-yr-old plantations (Fig. 2a and b), and N and P remaining of Eucalyptus litter in the 29-yr-old plantation rather than in the 8-yr-old plantation (Fig. 2c-f), but did not affect C, N and P remaining of Dicranopteris litter in the 8- and 29-yr-old plantations (Fig. 3). However, tree removal did not affect leaf litter C, N and P remaining of Eucalyptus and Dicranopteris both in the 8- and 29-yr-old plantations.
Fig. 1. The litter mass loss (%) of Eucalyptus and Dicranopteris and litter decomposition constant under different treatments, and the results (P values) of RMANOVA on the effects of understory removal (UR), tree removal (TR), and their interactions (UR*TR) on the litter mass loss (%) in the 8- (a, c and e) and 29yr-old (b, d and f) plantations. CK: control, no tree removal and no understory removal; UR: understory removal only; TR: tree removal only; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
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Fig. 2. Leaf litter C, N and P remaining (%) of Eucalyptus and the results (P values) of RM-ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on the nutrient mineralization in the 8- (a, c and e) and 29-yr-old (b, d and f) plantations. The fraction >100% means nutrient immobilization, and <100% means nutrient mineralization. CK: control; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
Moreover, the interactive effects of understory removal and tree removal on litter C, N and P remaining of Eucalyptus and Dicranopteris were not significant both in the 8- and 29-yr-old plantations. 3.4. The correlations of soil properties and litter decomposition parameters Regardless of stand age and plant species, the LML was negatively related to the C, N, P remaining (P ¼ 0.000, 0.013, and 0.024, respectively) and positively related to the initial litter C concentration (P ¼ 0.024; Table 3). Meanwhile, the C, N, P remaining were negatively related to the initial litter N:P ratio (P ¼ 0.046, 0.019, and 0.016; Table 3). When stand age and plant species were taken into consideration, in the 8-yr-old plantation, no correlations between the LML of Eucalyptus leaf litter and the measured soil properties was found (all P > 0.112, Table 4), except that C remaining was positively correlated to B (P ¼ 0.045). In addition, the LML of Dicranopteris was positively related to TMB, F and F:B ratio (P ¼ 0.026, 0.009 and 0.037, respectively), and C, N and P remaining were negatively correlated to TMB and B (all P < 0.044, Table 4). In the 29-yr-old plantation, the LML of Eucalyptus was positively related to SOC, soil N, soil C:N ratio, SMC, TMB, B and F (all P < 0.039, Table 4). And the C, N and P remaining were negatively related to SMC, TMB, B and F (all P < 0.030). In addition, the LML of Dicranopteris was positively related to F:B ratio and F (P ¼ 0.039 and 0.007, respectively). Meanwhile, the C remaining was negatively related to TMB and B (P ¼ 0.027 and 0.040, respectively; Table 4). 4. Discussion 4.1. Effects of understory removal on litter decomposition and nutrient mineralization Understory removal could affect litter decomposition through adjusting microbial biomass and microbial community structure (Wu et al., 2011; Zhao et al., 2012). In this study, understory removal decreased fungi biomass and total microbial
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Fig. 3. Leaf litter C, N and P remaining (%) of Dicranopteris, and the results (P values) of RM-ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on the nutrient mineralization in the 8- (a, c and e) and 29-yr-old (b, d and f) plantations. The fraction >100% means nutrient immobilization, and <100% means nutrient mineralization. CK: control; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
Table 3 The Pearson correlations (r) of initial litter properties and leaf litter decomposition and nutrient remaining in two studied plantations.
LML Litter Litter Litter Litter Litter Litter
C N P C:N C:P N:P
LML
C remaining
N remaining
P remaining
– 0.672* 0.251 0.471 0.225 0.359 0.563
0.882** 0.560 0.037 0.187 0.081 0.098 0.584*
0.692* 0.375 0.346 0.092 0.338 0.113 0.662*
0.645* 0.293 1.190 0.047 0.256 0.008 0.674*
Note: LML, litter C, litter N, litter P, litter C:N, C:P, N:P, C remaining, N remaining, and P remaining stand for the litter mass loss (%) at the end of the decomposition experiment; initial litter C, N and P concentrations; the ratios of initial litter C to N, C to P, and N to P concentrations; the litter carbon, nitrogen and phosphorus pool remaining (%) at the end of decomposition; respectively. * indicates P < 0.05, ** indicates P < 0.01.
biomass in the 29-yr-old plantation, and F:B ratio in two studied plantations. The effects of understory removal on fungal biomass and F:B ratio were detected at 1 and 2 years after treatments in the same experimental region (Wu et al., 2011). Fungi are the primary decomposing agents in forest ecosystems (Fukasawa et al., 2012). This probably explain why understory removal retarded the leaf litter decomposition of Eucalyptus in two studied plantations, and litter decomposition of Dicranopteris in the 29-yr-old plantation. Meanwhile, soil microclimate, which affected leaf litter decomposition (de Paz et al., 2018), could be influenced by understory vegetation. Similarly, Wang et al. (2014) found that soil temperature increased after understory removal in two subtropical lumber forests. However, Lei et al. (2018) reported that understory removal did not affect soil temperature and soil moisture content in subtropical Pinus massoniana plantations, probably due to higher stand density and canopy coverage. Previous study reported that high temperature facilitated litter decomposition (Rustad
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Table 4 The Pearson correlations (r) of soil properties, soil microbial biomass of different communities and leaf litter decomposition and nutrient remaining of Eucalyptus and Dicranopteris in the 8- and the 29-yr-old plantations. PT
Eucalyptus litter
Dicranopteris litter
LML
Cr
Nr
Pr
LML
Cr
Nr
Pr
8-yr-old
SOC TN C:N SMC TMB B F F:B
0.011 0.057 0.186 0.073 0.368 0.482 0.065 0.352
0.119 0.164 0.333 0.228 0.547 0.586* 0.217 0.072
0.008 0.060 0.254 0.115 0.534 0.571 0.240 0.031
0.377 0.314 0.083 0.269 0.157 0.297 0.223 0.425
0.142 0.266 0.511 0.017 0.636* 0.527 0.718** 0.606*
0.137 0.233 0.484 0.037 0.595* 0.590* 0.373 0.158
0.201 0.275 0.471 0.081 0.603* 0.642* 0.337 0.042
0.307 0.208 0.219 0.490 0.655* 0.784** 0.268 0.103
29-yr-old
SOC TN C:N SMC TMB B F F:B
0.597* 0.615* 0.731** 0.702* 0.738** 0.669* 0.841** 0.479
0.447 0.506 0.622* 0.628* 0.694* 0.643* 0.731** 0.374
0.471 0.538 0.651* 0.665* 0.744** 0.702* 0.791** 0.390
0.391 0.589* 0.536 0.623* 0.782** 0.766** 0.736** 0.268
0.601* 0.580* 0.591 0.531 0.475 0.375 0.733** 0.601*
0.315 0.311 0.369 0.172 0.634* 0.598* 0.492 0.002
0.312 0.273 0.519 0.126 0.563 0.518 0.486 0.084
0.070 0.190 0.256 0.374 0.219 0.223 0.015 0.291
Note: PT, LML, Cr, Nr, Pr, SOC, TN, C:N, SMC, TMB, B, F, and F:B stand for plantation types, the litter mass loss (%) at the end of the decomposition, initial litter carbon, nitrogen and phosphorus pool remaining (%) at the end of decomposition, soil organic carbon concentration, soil total nitrogen concentration, soil C:N ratio, soil moisture content, total soil microbial biomass, bacterial biomass, fungi biomass and the ratio of fungi to bacterial biomass at the start of decomposition, respectively. * indicates P < 0.05, ** indicates P < 0.01.
and Fernandez, 1998; Bothwell et al., 2014), but such effect was not observed in the present study. Therefore, understory vegetation affected leaf litter decomposition primarily by altering soil microbial communities in the studied plantations. Leaf litter C, N and P remaining was related to the leaf litter mass loss. It was supported by the negative correlations between nutrient remaining and the litter mass loss. Thus, the significant effects of understory removal on litter C, N and P remaining of Eucalyptus could be ascribed to the more significant effects of understory removal on Eucalyptus leaf litter mass loss in the 29-yr-old plantation. In addition, no significant correlations between C, N and P remaining of Dicranopteris and soil microbial biomass in the 29-yr-old plantation, low litter decomposition rate of Dicranopteris and its high N and P utilization rates (Russell et al., 1998; Chen et al., 2016), could be responsible for the insignificant effects of understory removal on the litter nutrient mineralization or immobilization of Dicranopteris. The dynamics of litter C was consistent with the results reported by Zhu et al. (2016). However, the dynamics of litter N and P showed alternate immobilization or mineralization patterns in two studied plantations. It could be mainly caused by microbial demand for N and P (Bani et al., 2018). Ribeiro et al. (2002) found the litter N immobilization in Eucalyptus globulus plantations. In addition, N immobilization was also found at the early stage of decomposition in the other studies (Demessie et al., 2012; Pant et al., 2017). Thus, soil fertility could be responsible for the patterns of nutrient immobilization or mineralization (Bonanomi et al., 2017). 4.2. Effects of tree removal on litter decomposition and nutrient mineralization The previous study indicated that eliminating tree rhizosphere C input decreased litter decomposition (Subke et al., 2004). However, Wu et al. (2011) reported much weaker effect of tree on litter decomposition than understory plant at 1e2 years after treatment in the studied plots. In this study, the non-significant effect of tree removal on soil temperature, soil moisture content, soil microbial biomass, and microbial community composition in two studied plantations could be explained why leaf litter decomposition and nutrient dynamics were not affected by treatments (Schneider et al., 2012; Petraglia et al., 2019). In addition, tree removal was approximately equivalent to thinning as the small area of subplots in the present study. BravoOviedo et al. (2017) reported that intermediate canopy reduction did not reduce decomposition in an oak forest. Therefore, the effects of tree removal on soil microclimate, soil microbial biomass and microbial community may be compensated by understory vegetation to some extent. 4.3. Effects of stand age and plant species on litter decomposition and nutrient mineralization Stand age influenced litter initial chemical properties. The N concentration was higher in the 29-yr-old plantation than that in the 8-yr-old plantation. The result was consistent with the previous report (Fan et al., 2015). The previous study showed a positive correlation between initial litter N concentration and litter decomposition rate (Szefer et al., 2017). However, Bachega et al. (2016) proposed that the initial litter N was not applied to predict litter decomposition rate. In this study, although the significant correlation between initial litter N concentration and leaf litter decomposition rate was not observed, the leaf litter decomposition rate was faster in the 29-yr-old plantation with higher initial litter N concentration
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than that in the 8-yr-old plantation. Meanwhile, soil moisture content was more important than soil temperature in driving litter decomposition in the 29-yr-old plantation, suggesting the dominant roles of soil moisture in microbial-mediated carbon decomposition process (Singh et al., 1999; Wang et al., 2019). In addition, the relative higher microbial biomass in the 29-yrold plantation could facilitate leaf litter decomposition. Therefore, the initial litter N concentration, soil moisture content, and soil microbial biomass could be responsible for diverse responses of decomposition rate in the 8- and 29-yr-old plantations. The nutrient remaining was negatively relative to leaf litter decomposition rate (Table 3). As a result, these factors could be responsible to the more significant effects of understory removal on nutrient remaining in the 29-yr-old plantation than in the 8-yr-old plantation. The leaf litter decomposition rate and nutrient remaining of Eucalyptus and Dicranopteris made different responses to understory removal. It could be ascribed to plant traits (Cornwell et al., 2008). Plant species, even genotypes influenced litter initial chemical properties (Ge et al., 2017; Mikola et al., 2018). In addition, litter quality was lower in Dicranopteris with high lignin content and lignin:N ratio than in Eucalyptus (Ma et al., 2009; Stewart et al., 2011). It was also supported by the higher decomposition constant of Eucalyptus than that of Dicranopteris. The litter decomposition constant of Eucalyptus in the control plots (0.56e0.59 yr-1) was similar to previous results from the close-by sites (0.51e0.77 yr1; Zhu et al., 2016). The litter decomposition constant of Dicranopteris in the control plots was 0.30e0.31 yr-1, which was also close to the result from the subtropics (0.25 yr-1; Ma et al., 2009). Furthermore, different species could make diverse responses to one disturbance (e.g., understory removal, Wright et al., 2015). Sun et al. (2017) reported that the survival of Castanopsis fissa seedlings in understory removal was significantly higher, while the Schima superba and Michelia macclurei seedlings were not sensitive to understory removal. Understory removal and tree removal could affect the litter quality (Henneron et al., 2018). However, in the present study, the initial leaf litter was exclusive of that from the understory/tree removal subplots. Therefore, the results could be limited to effects on the leaf litter from the control subplots. 5. Conclusion This study suggested that understory removal significantly reduced litter decomposition and litter C mineralization of Eucalyptus both in the 8- and 29-yr-old plantations, and significantly reduced N and P mineralization of Eucalyptus litter only in the 29-yr-old plantation. In contrast, it significantly decreased litter decomposition of Dicranopteris only in the 29-yr-old plantation, and did not affect C, N and P mineralization of Dicranopteris litter. Surprisingly, tree removal did not show any significant effect on litter decomposition and nutrient mineralization. Our results indicate that the effects of understory plants on leaf litter decomposition and nutrient mineralization is more significant than overstory trees, and it can be altered by stand age and plant species. These findings could promote the understanding of ecological processes of litter decomposition and nutrient mineralization in plantation forest ecosystems. Conflicts of interest The authors declare that they have no conflicts of interest. Acknowledgements This work was supported by the National Natural Science Foundation of China (41571249, 41771278, U1701246), the Hunan Provincial Natural Science Foundation of China (2017JJ3083), Science and Technology Program of Guangzhou, China (201707010344), Youth Innovation Promotion Association CAS, Open Foundation of the State Key Laboratory of Urban and Regional Ecology of China (SKLURE2016-2-5), and the Research Foundation of Education Bureau of Hunan Province, China (17B099). Special thanks to Mr. Mozheng Li, Shengxing Fu and Dr. Xiaomin Zhu for their helps in leaf litter collection and litterbags preparation. We are grateful to Dr. Arjun Pandey for editing the English language. References Aponte, C., García, L.V., Maranon, T., 2012. Tree species effect on litter decomposition and nutrient release in Mediterranean oak forests changes over time. Ecosystems 15, 1204e1218. Bååth, E., Anderson, T.H., 2003. 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Original Research Article
Stand age and species traits alter the effects of understory removal on litter decomposition and nutrient dynamics in subtropical Eucalyptus plantations Yuanqi Chen a, b, e, Yanju Zhang b, c, Jianbo Cao b, c, Shenglei Fu d, Shuijin Hu e, Jianping Wu f, Jie Zhao g, Zhanfeng Liu b, * a
Hunan Province Key Laboratory of Coal Resources Clean-utilization and Mine Environment Protection, Hunan University of Science and Technology, Xiangtan, 411201, China Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China c University of Chinese Academy of Sciences, Beijing, 100049, China d College of Environment and Planning, Henan University, Kaifeng, 475004, China e Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695, United States f School of Ecology and Environmental Science, Yunnan University, Kunming, 650091, China g Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 April 2019 Received in revised form 21 June 2019 Accepted 21 June 2019
Litter decomposition is a crucial ecological process that regulates nutrient cycling. However, the effects of understory plants and overstory trees on litter decomposition and nutrient dynamics are still poorly understood. We conducted understory plants removal and/or overstory trees removal to examine the resulting effects on litter decomposition and nutrient mineralization in two Eucalyptus plantations with contrasting ages (8-yr-old, 29-yr-old) in subtropical China. Litter bags containing naturally senesced leaves of either overstory Eucalyptus urophylla or understory Dicranopteris dichotoma were placed in field and periodically collected for analyses of carbon (C), nitrogen (N), phosphorus (P) and calculation of mass loss. Our results showed that understory plants removal significantly reduced litter decomposition of E. urophylla in both plantations, but N and P mineralization were reduced only in the 8-yr-old plantation. In contrast, it reduced litter decomposition of D. dichotoma only in the 29-yr-old plantation, but had no effects on N and P mineralization in either plantation. In comparison, overstory tree removal did not have any effects on decomposition or mineralization of N and P of E. urophylla and D. dichotoma litters. These results indicate that the role of understory plants in mediating litter decomposition and nutrient mineralization is more important than overstory trees, and it can be altered by stand age and plant species. Our findings could facilitate the understanding of ecological processes of litter decomposition and nutrient mineralization in subtropical forest ecosystems. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords: Leaf litter Understory plant Nutrient mineralization Subtropical forest Stand age Plant identity
* Corresponding author. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, No. 723, Xingke Road, Guangzhou, 510650, China. E-mail address: [email protected] (Z. Liu). https://doi.org/10.1016/j.gecco.2019.e00693 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
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1. Introduction Litter decomposition is a fundamental ecological process that regulates nutrient cycling (Versini et al., 2014; Bravo-Oviedo et al., 2017), and is also a key determinant controlling carbon (C) cycling in forest ecosystems (Creamer et al., 2015). When litter decomposes, the litter-derived C could be incorporated into microbial biomass and/or be respired, simultaneously, the input of litter-derived C could stimulate soil organic C decomposition by altering soil microbial activity and community structure (Cotrufo et al., 2015). In reverse, the soil microbial biomass and microbial community structure could impact litter decomposition (Schneider et al., 2012; Müller et al., 2017). Besides, soil microclimate and litter quality also affect litter decomposition process (Petraglia et al., 2019) and can explain over 31% of the variance in litter decomposition in subtropical plantations (Seidelmann et al., 2016). In subtropical forest ecosystems, understory plants play a critical role in sustaining soil microclimate and driving ecological processes, especially in plantation forests with a large understory plant biomass (Zhao et al., 2012). The understory biomass was above 17 Mg ha1 and contributed 18.7e46.6% of the plant carbon pool in subtropical plantations (Chen et al., 2015; Fan et al., 2015). Wang et al. (2014) found that understory removal significantly reduced soil nitrogen (N) mineralization and nitrification rates in two subtropical lumber plantations. Our previous studies found that understory plants made a significant contribution to soil respiration, soil food web structure, litter decomposition, and net ecosystem productivity in subtropical plantations (Zhao et al., 2012; Wu et al., 2014). However, most studies mainly focused on the tree leaf litters, and few attention has been paid to the leaf litters of understory plant in forest ecosystems (Aponte et al., 2012; Schuster and Dukes, 2014). In China, plantation area of approximately 69 million hectares is one third of that of the world with over 60% of that distributed in subtropics (China Forestry Database; Wang et al., 2010). Eucalyptus plantations is approximately 34% of the total plantation area in southern China, which cover 4.50 million hectares as Eucalyptus trees have high productivity and rapid economic returns (China Forestry Database; China Science Daily, 2015). Understory plant, which was dominated by Dicranopteris, contributed up to 33.9% of the net primary production of the Eucalyptus plantations in southern China (Wu et al., 2014). However, understory removal is still a common practice to prevent fire and eliminate the competition with target tree species in forest management (Campbell et al., 2012; Zhou et al., 2018). To our knowledge, little is known about the litter decomposition process and nutrient dynamics of understory plant in such ecosystem. Moreover, the responses of litter decomposition and nutrient dynamics of understory plant to the removal of overstory trees are not well understood. Forest age also plays an important role in controlling litter decomposition (Skorupa et al., 2015). Microclimate, litter quality and soil microbial community composition will vary with forest age and result in various responses of litter decomposition to disturbance (i.e., understory removal, overstory thinning) consequently (Trap et al., 2013; Wu et al., 2013; Trogisch et al., 2016; Yin et al., 2016). Our previous study also found that understory plants removal altered the fate of soil labile C in the plantations of different ages (Chen et al., 2019). However, there is still knowledge gap about how the loss of understory plants and/or overstory trees respectively impact litter decomposition and nutrient dynamics in forests of different ages (Qiao et al., 2014). In this study, understory removal and/or tree removal were conducted in two Eucalyptus plantations of contrasting stand ages (8- and 29-yr-old). We hypothesized that (1) tree removal and understory removal would retard litter decomposition and nutrient dynamics by changing the composition of soil microbial community and soil microclimate; (2) the effects of tree removal and understory removal on litter decomposition and nutrient dynamics depend on stand age and plant species due to their effects on soil microclimate and litter quality. 2. Materials and methods 2.1. Study site This experiment was carried out at the Heshan National Field Observation and Research Station of Forest Ecosystem (112.83 E, 22.57 N), which is located in Heshan city, Guangdong Province in southern China. The mean altitude is 80 m. The climate in this region is a typical subtropical monsoon climate with a distinct wet and dry season (Chen et al., 2015). The mean annual temperature is 22.3 C, and the mean precipitation is 1688 mm yr1 during 2005e2012. The soil is classified as Ultisol (Chen et al., 2015). The studied Eucalyptus plantations were established on homogenous degraded hilly lands, and Eucalyptus urophylla were planted at a spacing of 3 m 2 m in 2005 and 1984, respectively. In these two plantations, understory plants were highly dominated by Dicranopteris dichotoma. The details of understory plants were reported in Wu et al. (2011). 2.2. Experimental design Experimental plots were established in late winter of 2007 with three replicated plots in both 8- and 29-yr-old plantations (Wu et al., 2011). The nearest distance of plots was more than 100 m away from each other. Tree girdling and understory removal were conducted respectively or jointly in each plantation in 2007. Understory plants were removed by harvesting aboveground parts of plants and the new understory plant growth was removed monthly by hand as some of them can sprout and grow from remnant roots in the subplots with understory removal. Each plot (10 m 10 m) was
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divided into four subplots, which corresponded to four treatments. The details of plots has been described in Wu et al. (2011). This study was conducted in 2013, tree girdling was equivalent to tree removal as the girdled trees died after 1 year of treatment and then removed out of subplots. That is, four treatments in this study included: (1) no tree removal and no understory removal (CK), (2) understory removal only (UR), (3) tree removal only (TR), and (4) understory removal and tree removal (TUR). 2.3. Leaf litter decomposition experiment The fresh leaf litter of Eucalyptus and Dicranopteris was respectively collected from two studied plantations with understory plant and overstory tree on April 2013. Thereafter, all leaf litters of each species from the same plantation were mixed homogeneously and placed into litter bags (20 cm 20 cm) made from polyvinyl screen. To alleviate the effect of mesh size of litter bag on soil biota and insects, the mesh size of one side was 0.5 mm and the other side was 2.0 mm, which was faced up in order to enable access for some soil biota and insects (Melillo et al., 1982). Each bag was filled with 8.0 g (oven-dried weight) leaf litter of Eucalyptus or Dicranopteris. Six litter bags containing the leaf litter of each species were placed on the soil surface in each subplot. In total, 288 litter bags were prepared for decomposition. The decomposition of leaf litter started on 17 May, 2013 and lasted 17 months. Every two bags (one with leaf litter of Eucalyptus, another with leaf litter of Dicranopteris) were retrieved from each subplot firstly on 18 July 2013, and then quarterly on 22 October 2013, 16 January 2014, 21 April 2014, 15 July 2014, and 17 October 2014, respectively. The retrieved litters were cleaned using forceps, dried in an oven at 65 C for 72 h, and then weighted to calculate the percentage of litter mass loss (LML). Decomposition rate of leaf litter was determined by the percentage of litter mass loss. LML (%) ¼ (8.0 - interval weight of litter) 100/8.0, where the 8.0 is the initial weight of litter in each bag. Meanwhile, the C, N and P concentration of retrieved litters were determined by using potassium dichromate oxidation method, Kjeldahl method, and the Mo-Sb colorimetric method, respectively (Bao, 2000). In all subplots, soil temperatures at the 0e5 cm soil layer were recorded by button thermometers (LI-COR Biosciences, Lincoln, NE, USA) from Aug. 2014 to Jun. 2015. 2.4. Soil sampling and analysis At the start of litter decomposition experiment, soil sample (0e20 cm depth) was collected with five cores (3.0 cm inner diameter) and combined into a composite sample for each subplot. In total, 24 samples were collected. The litter on soil surface was removed carefully when soil sample was taken. Soils were thoroughly homogenized by sieving with 2 mm mesh. Visible plant roots, rocks, and soil macrofauna in soils were removed by hand before analysis. Soil organic C (SOC) concentration was determined with the traditional potassium dichromate oxidation method (Bao, 2000). Soil moisture content (SMC %, moisture content per 100 g dry soil) was measured by oven-drying for 24 h at 105 C. N and P concentrations of soil and litter were determined with Kjeldahl method, and sulfuric acid solution and Mo-Sb Antispectrophotometer method, respectively (Bao, 2000). Soil microbial community was characterized by using phospholipid fatty acids (PLFAs) analysis as described by Bossio and Scow (1998). Concentration of each PLFA was calculated based on 19:0 internal standard concentration. PLFAs used as bacterial biomarkers were i15:0, a15:0, i16:0, 18:1u7, i17:0, a17:0, cy17:0, cy19:0; the PLFAs used as fungal biomarkers were 18:1u9c and 18:2u6,9c, and total microbial biomass was considered to be represented by bacterial biomarkers, fungal biomarkers, and other PLFAs such as 16:1u5c, 10 Me 16:0, 10 Me 17:0, 10 Me 18:0 (Frostegård and Bååth, 1996; Bååth and Anderson, 2003; Joergensen and Wichern, 2008). 2.5. Data analysis Nutrient remaining (%) was calculated by dividing remaining and initial nutrient pool. Meanwhile, an exponential decay model was used to analyze the relationship between initial litter remains and decomposition time: X ¼ a*e-kt, where X is the fraction of initial litter remains at time t (yr), a is the simulation parameter, e is the base of natural logarithm, k is the decomposition constant (yr1) over the whole decomposition period. One-way ANOVA was performed to explore the difference in initial properties of leaf litter between the 8- and 29-yr-old plantations, and soil properties among different treatments at the start of litter decomposition experiment in two plantations. T-test was carried out when the data could not meet the requirements of one-way ANOVA. Two-way ANOVA was employed to test the effects of understory removal and tree removal on soil microbial community in the 8- and 29-yr-old plantations. RMANOVA was used to test the effects of understory removal and tree removal on leaf litter decomposition, nutrient dynamics, and soil temperature in two plantations. In addition, the effects of stand age, understory removal and tree removal on soil temperature and soil moisture content were analyzed by three-way ANOVA. The effects of stand age, plant species, understory removal and tree removal on the LML and decomposition constant (k) were tested by four-way ANOVA. Pearson correlation analyses were employed to test the relationships between soil properties (i.e., physicochemical properties and soil microbial communities) and decomposition indices (i.e., the LML and the fraction of litter C, N, and P remaining at the end of experiment) in two studied plantations. All statistical analyses were carried out with SPSS 18 (SPSS, Inc, Chicago, IL) and statistical significance was determined at P < 0.05 level.
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Table 1 Results of two-way ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on total soil microbial biomass (TMB), bacterial biomass (B), fungi biomass (F), fungi: bacteria ratio (F:B) (biomass expressed as PLFAs) in the 0e10 cm soil layer, the concentration of soil organic carbon (SOC) and soil nitrogen (TN), soil C:N ratio, and soil moisture content (SMC) in 0e20 cm soil layer at the start of litter decomposition experiment, and soil temperature (ST) in 0e5 cm soil layer during Aug. 2014 to Jun. 2015 in the 8- and 29-yr-old plantations. 8-yr-old
29-yr-old
UR
TMB B F F:B SOC TN C:N ST SMC
TR
UR*TR
UR
TR
UR*TR
F
P
F
P
F
P
F
P
F
P
F
P
0.21 0.00 3.03 5.08 0.24 0.03 1.34 0.69 0.75
0.661 0.992 0.120 0.054 0.638 0.874 0.280 0.430 0.412
0.66 0.44 0.26 0.00 0.00 0.01 0.10 0.17 0.56
0.442 0.524 0.626 0.961 0.990 0.939 0.765 0.688 0.476
0.00 0.00 0.08 0.39 0.04 0.02 0.02 1.46 0.39
0.999 0.992 0.873 0.550 0.847 0.893 0.886 0.262 0.549
6.31 4.27 17.96 5.08 8.31 3.15 0.68 20.94 8.35
0.036 0.073 0.003 0.054 0.020 0.114 0.434 0.002 0.020
0.29 0.27 0.11 0.37 0.31 1.39 0.27 0.75 0.25
0.605 0.621 0.749 0.560 0.590 0.272 0.617 0.412 0.632
0.27 0.17 0.08 0.53 0.46 0.96 0.03 0.28 1.90
0.615 0.688 0.780 0.489 0.517 0.355 0.875 0.611 0.205
3. Results
3.1. Soil characteristics and initial litter quality 3.1.1. Soil characteristics Understory removal significantly decreased total microbial biomass (TMB) and fungal biomass (F), and decreased the bacterial biomass (B) and F:B ratio to some extent in the 29-yr-old plantation (Table 1). Surprisingly, the significant effects or trends were not observed, except that the F:B ratio showed a decreased trend in the 8-yr-old plantation. Furthermore, tree removal did not show any significant effect on composition of soil microbial community in two studied plantations (Table 1). Understory removal significantly decreased soil C concentration in the 29-yr-old plantation, but not in the 8-yr-old plantation. Soil N and soil C:N ratio were not affected by understory removal and tree removal both in the 8- and 29-yr-old plantations (Table 1). Understory removal significantly increased soil temperature and decreased soil moisture content in the 29-yr-old plantation, but not in the 8-yr-old plantation. Meanwhile, tree removal did not affect them both in the 8- and 29-yr-old plantations (Table 1). Soil temperature in the 8-yr-old plantation was higher than that in the 29-yr-old plantation (P ¼ 0.001). Conversely, soil moisture content was lower in the 8-yr-old plantation than in the 29-yr-old plantation (P < 0.001). The interaction effects of understory removal, tree removal and stand age on soil temperature and soil moisture content were not significant (all P > 0.210). 3.1.2. Initial litter quality The higher litter C concentration and C:P ratio, lower N and P concentration of Eucalyptus than that of Dicranopteris were detected both in the 8- and 29-yr-old plantations (Table 2). In addition, the litter P concentration of Eucalyptus was lower in the 8-yr-old plantation than that in the 29-yr-old plantation (P ¼ 0.010), but there was no significant difference in litter C, N, C:N ratio of Eucalyptus between two plantations (P ¼ 0.051, 0.082, and 0.905, respectively). The litter C, N, and P concentrations of Dicranopteris were lower (P ¼ 0.049, <0.001, and 0.040, respectively), but C:N ratio was higher (P ¼ 0.001) in the 8yr-old plantation than that in the 29-yr-old plantation (Table 2).
Table 2 The initial chemical properties of leaf litter in the 8- and the 29-yr-old plantations (mean ± SE, n ¼ 3). C, N and P (%) are the concentrations of total carbon, nitrogen and phosphorus in the leaf litter; C:N, C:P, and N:P are the ratios of carbon to nitrogen, carbon to phosphorus, and nitrogen to phosphorus concentrations in the leaf litter. Properties
C (%) N (%) P (%) C:N C:P N:P
8-yr-old
P value
E. urophylla
D. dichotoma
51.59 ± 1.10 A 0.73 ± 0.05 A 0.025 ± 0.001 B 70.48 ± 9.95 A 2037 ± 74.4 A 30.03 ± 1.91 A
45.80 ± 0.76 b 0.98 ± 0.02 b 0.037 ± 0.002 b 46.67 ± 1.15 a 1253 ± 76.4 a 26.97 ± 2.36 a
0.020 0.012 0.010 0.248 0.006 0.371
(20.60) (19.47) (21.39) (2.38) (47.66) (1.02)
29-yr-old
P value
E. urophylla
D. dichotoma
55.24 ± 1.16 A 0.92 ± 0.06 A 0.03 ± 0.001 A 60.53 ± 5.65 A 1856 ± 73.5 A 31.02 ± 2.09 A
48.05 ± 0.25 a 1.47 ± 0.03 a 0.048 ± 0.00 a 32.72 ± 0.85 b 994.3 ± 10.9 a 30.40 ± 0.45 a
0.004 0.002 0.000 0.036 0.006 0.789
(36.55) (59.42) (756.3) (4.86) (2.09) (0.08)
P values are from one-way ANOVA of species in the plantation with the same stand age. The different uppercase and lowercase letters mean significant differences between 8- and 29-yr-old plantations for the leaf litter of E. urophylla and D. dichotoma, respectively.
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3.2. Leaf litter decomposition Leaf litter decomposition was represented by the percentage of litter mass loss (LML). Two-way RM ANOVA indicated that understory removal significantly decreased the LML of Eucalyptus in the 8- and 29-yr-old plantation (Fig. 1a and b), and the LML of Dicranopteris in the 29-yr-old plantation (Fig. 1d). However, tree removal did not show significant effects on the LML of Eucalyptus and Dicranopteris in the 8- and 29-yr-old plantations. Four-way RM ANOVA showed that stand age, plant species, and understory removal significant affected the LML (all P < 0.001), yet tree removal did not (P > 0.05). The interaction effect of stand age and understory removal, and the interaction effect of plant species and understory removal on the LML were significant (P ¼ 0.001, and P < 0.001, respectively), but other interaction effects were not significant (all P > 0.116). Understory removal and plant species significantly affected leaf litter decomposition constant (four-way ANOVA, P < 0.001), but stand age and tree removal did not (P > 0.05). Leaf litter decomposition constant was lower when the understory plants was absent (Fig. 1e and f). The interaction effects of understory removal, tree removal, stand age, and plant species on decomposition constant were not significant (P > 0.05). 3.3. Nutrient mineralization Understory removal significantly increased C remaining of Eucalyptus litter both in the 8- and 29-yr-old plantations (Fig. 2a and b), and N and P remaining of Eucalyptus litter in the 29-yr-old plantation rather than in the 8-yr-old plantation (Fig. 2c-f), but did not affect C, N and P remaining of Dicranopteris litter in the 8- and 29-yr-old plantations (Fig. 3). However, tree removal did not affect leaf litter C, N and P remaining of Eucalyptus and Dicranopteris both in the 8- and 29-yr-old plantations.
Fig. 1. The litter mass loss (%) of Eucalyptus and Dicranopteris and litter decomposition constant under different treatments, and the results (P values) of RMANOVA on the effects of understory removal (UR), tree removal (TR), and their interactions (UR*TR) on the litter mass loss (%) in the 8- (a, c and e) and 29yr-old (b, d and f) plantations. CK: control, no tree removal and no understory removal; UR: understory removal only; TR: tree removal only; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
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Fig. 2. Leaf litter C, N and P remaining (%) of Eucalyptus and the results (P values) of RM-ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on the nutrient mineralization in the 8- (a, c and e) and 29-yr-old (b, d and f) plantations. The fraction >100% means nutrient immobilization, and <100% means nutrient mineralization. CK: control; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
Moreover, the interactive effects of understory removal and tree removal on litter C, N and P remaining of Eucalyptus and Dicranopteris were not significant both in the 8- and 29-yr-old plantations. 3.4. The correlations of soil properties and litter decomposition parameters Regardless of stand age and plant species, the LML was negatively related to the C, N, P remaining (P ¼ 0.000, 0.013, and 0.024, respectively) and positively related to the initial litter C concentration (P ¼ 0.024; Table 3). Meanwhile, the C, N, P remaining were negatively related to the initial litter N:P ratio (P ¼ 0.046, 0.019, and 0.016; Table 3). When stand age and plant species were taken into consideration, in the 8-yr-old plantation, no correlations between the LML of Eucalyptus leaf litter and the measured soil properties was found (all P > 0.112, Table 4), except that C remaining was positively correlated to B (P ¼ 0.045). In addition, the LML of Dicranopteris was positively related to TMB, F and F:B ratio (P ¼ 0.026, 0.009 and 0.037, respectively), and C, N and P remaining were negatively correlated to TMB and B (all P < 0.044, Table 4). In the 29-yr-old plantation, the LML of Eucalyptus was positively related to SOC, soil N, soil C:N ratio, SMC, TMB, B and F (all P < 0.039, Table 4). And the C, N and P remaining were negatively related to SMC, TMB, B and F (all P < 0.030). In addition, the LML of Dicranopteris was positively related to F:B ratio and F (P ¼ 0.039 and 0.007, respectively). Meanwhile, the C remaining was negatively related to TMB and B (P ¼ 0.027 and 0.040, respectively; Table 4). 4. Discussion 4.1. Effects of understory removal on litter decomposition and nutrient mineralization Understory removal could affect litter decomposition through adjusting microbial biomass and microbial community structure (Wu et al., 2011; Zhao et al., 2012). In this study, understory removal decreased fungi biomass and total microbial
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Fig. 3. Leaf litter C, N and P remaining (%) of Dicranopteris, and the results (P values) of RM-ANOVA on the effects of understory removal (UR), tree removal (TR) and their interactions (UR*TR) on the nutrient mineralization in the 8- (a, c and e) and 29-yr-old (b, d and f) plantations. The fraction >100% means nutrient immobilization, and <100% means nutrient mineralization. CK: control; TUR: tree removal plus understory removal. Values are mean ± SE, n ¼ 3.
Table 3 The Pearson correlations (r) of initial litter properties and leaf litter decomposition and nutrient remaining in two studied plantations.
LML Litter Litter Litter Litter Litter Litter
C N P C:N C:P N:P
LML
C remaining
N remaining
P remaining
– 0.672* 0.251 0.471 0.225 0.359 0.563
0.882** 0.560 0.037 0.187 0.081 0.098 0.584*
0.692* 0.375 0.346 0.092 0.338 0.113 0.662*
0.645* 0.293 1.190 0.047 0.256 0.008 0.674*
Note: LML, litter C, litter N, litter P, litter C:N, C:P, N:P, C remaining, N remaining, and P remaining stand for the litter mass loss (%) at the end of the decomposition experiment; initial litter C, N and P concentrations; the ratios of initial litter C to N, C to P, and N to P concentrations; the litter carbon, nitrogen and phosphorus pool remaining (%) at the end of decomposition; respectively. * indicates P < 0.05, ** indicates P < 0.01.
biomass in the 29-yr-old plantation, and F:B ratio in two studied plantations. The effects of understory removal on fungal biomass and F:B ratio were detected at 1 and 2 years after treatments in the same experimental region (Wu et al., 2011). Fungi are the primary decomposing agents in forest ecosystems (Fukasawa et al., 2012). This probably explain why understory removal retarded the leaf litter decomposition of Eucalyptus in two studied plantations, and litter decomposition of Dicranopteris in the 29-yr-old plantation. Meanwhile, soil microclimate, which affected leaf litter decomposition (de Paz et al., 2018), could be influenced by understory vegetation. Similarly, Wang et al. (2014) found that soil temperature increased after understory removal in two subtropical lumber forests. However, Lei et al. (2018) reported that understory removal did not affect soil temperature and soil moisture content in subtropical Pinus massoniana plantations, probably due to higher stand density and canopy coverage. Previous study reported that high temperature facilitated litter decomposition (Rustad
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Table 4 The Pearson correlations (r) of soil properties, soil microbial biomass of different communities and leaf litter decomposition and nutrient remaining of Eucalyptus and Dicranopteris in the 8- and the 29-yr-old plantations. PT
Eucalyptus litter
Dicranopteris litter
LML
Cr
Nr
Pr
LML
Cr
Nr
Pr
8-yr-old
SOC TN C:N SMC TMB B F F:B
0.011 0.057 0.186 0.073 0.368 0.482 0.065 0.352
0.119 0.164 0.333 0.228 0.547 0.586* 0.217 0.072
0.008 0.060 0.254 0.115 0.534 0.571 0.240 0.031
0.377 0.314 0.083 0.269 0.157 0.297 0.223 0.425
0.142 0.266 0.511 0.017 0.636* 0.527 0.718** 0.606*
0.137 0.233 0.484 0.037 0.595* 0.590* 0.373 0.158
0.201 0.275 0.471 0.081 0.603* 0.642* 0.337 0.042
0.307 0.208 0.219 0.490 0.655* 0.784** 0.268 0.103
29-yr-old
SOC TN C:N SMC TMB B F F:B
0.597* 0.615* 0.731** 0.702* 0.738** 0.669* 0.841** 0.479
0.447 0.506 0.622* 0.628* 0.694* 0.643* 0.731** 0.374
0.471 0.538 0.651* 0.665* 0.744** 0.702* 0.791** 0.390
0.391 0.589* 0.536 0.623* 0.782** 0.766** 0.736** 0.268
0.601* 0.580* 0.591 0.531 0.475 0.375 0.733** 0.601*
0.315 0.311 0.369 0.172 0.634* 0.598* 0.492 0.002
0.312 0.273 0.519 0.126 0.563 0.518 0.486 0.084
0.070 0.190 0.256 0.374 0.219 0.223 0.015 0.291
Note: PT, LML, Cr, Nr, Pr, SOC, TN, C:N, SMC, TMB, B, F, and F:B stand for plantation types, the litter mass loss (%) at the end of the decomposition, initial litter carbon, nitrogen and phosphorus pool remaining (%) at the end of decomposition, soil organic carbon concentration, soil total nitrogen concentration, soil C:N ratio, soil moisture content, total soil microbial biomass, bacterial biomass, fungi biomass and the ratio of fungi to bacterial biomass at the start of decomposition, respectively. * indicates P < 0.05, ** indicates P < 0.01.
and Fernandez, 1998; Bothwell et al., 2014), but such effect was not observed in the present study. Therefore, understory vegetation affected leaf litter decomposition primarily by altering soil microbial communities in the studied plantations. Leaf litter C, N and P remaining was related to the leaf litter mass loss. It was supported by the negative correlations between nutrient remaining and the litter mass loss. Thus, the significant effects of understory removal on litter C, N and P remaining of Eucalyptus could be ascribed to the more significant effects of understory removal on Eucalyptus leaf litter mass loss in the 29-yr-old plantation. In addition, no significant correlations between C, N and P remaining of Dicranopteris and soil microbial biomass in the 29-yr-old plantation, low litter decomposition rate of Dicranopteris and its high N and P utilization rates (Russell et al., 1998; Chen et al., 2016), could be responsible for the insignificant effects of understory removal on the litter nutrient mineralization or immobilization of Dicranopteris. The dynamics of litter C was consistent with the results reported by Zhu et al. (2016). However, the dynamics of litter N and P showed alternate immobilization or mineralization patterns in two studied plantations. It could be mainly caused by microbial demand for N and P (Bani et al., 2018). Ribeiro et al. (2002) found the litter N immobilization in Eucalyptus globulus plantations. In addition, N immobilization was also found at the early stage of decomposition in the other studies (Demessie et al., 2012; Pant et al., 2017). Thus, soil fertility could be responsible for the patterns of nutrient immobilization or mineralization (Bonanomi et al., 2017). 4.2. Effects of tree removal on litter decomposition and nutrient mineralization The previous study indicated that eliminating tree rhizosphere C input decreased litter decomposition (Subke et al., 2004). However, Wu et al. (2011) reported much weaker effect of tree on litter decomposition than understory plant at 1e2 years after treatment in the studied plots. In this study, the non-significant effect of tree removal on soil temperature, soil moisture content, soil microbial biomass, and microbial community composition in two studied plantations could be explained why leaf litter decomposition and nutrient dynamics were not affected by treatments (Schneider et al., 2012; Petraglia et al., 2019). In addition, tree removal was approximately equivalent to thinning as the small area of subplots in the present study. BravoOviedo et al. (2017) reported that intermediate canopy reduction did not reduce decomposition in an oak forest. Therefore, the effects of tree removal on soil microclimate, soil microbial biomass and microbial community may be compensated by understory vegetation to some extent. 4.3. Effects of stand age and plant species on litter decomposition and nutrient mineralization Stand age influenced litter initial chemical properties. The N concentration was higher in the 29-yr-old plantation than that in the 8-yr-old plantation. The result was consistent with the previous report (Fan et al., 2015). The previous study showed a positive correlation between initial litter N concentration and litter decomposition rate (Szefer et al., 2017). However, Bachega et al. (2016) proposed that the initial litter N was not applied to predict litter decomposition rate. In this study, although the significant correlation between initial litter N concentration and leaf litter decomposition rate was not observed, the leaf litter decomposition rate was faster in the 29-yr-old plantation with higher initial litter N concentration
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than that in the 8-yr-old plantation. Meanwhile, soil moisture content was more important than soil temperature in driving litter decomposition in the 29-yr-old plantation, suggesting the dominant roles of soil moisture in microbial-mediated carbon decomposition process (Singh et al., 1999; Wang et al., 2019). In addition, the relative higher microbial biomass in the 29-yrold plantation could facilitate leaf litter decomposition. Therefore, the initial litter N concentration, soil moisture content, and soil microbial biomass could be responsible for diverse responses of decomposition rate in the 8- and 29-yr-old plantations. The nutrient remaining was negatively relative to leaf litter decomposition rate (Table 3). As a result, these factors could be responsible to the more significant effects of understory removal on nutrient remaining in the 29-yr-old plantation than in the 8-yr-old plantation. The leaf litter decomposition rate and nutrient remaining of Eucalyptus and Dicranopteris made different responses to understory removal. It could be ascribed to plant traits (Cornwell et al., 2008). Plant species, even genotypes influenced litter initial chemical properties (Ge et al., 2017; Mikola et al., 2018). In addition, litter quality was lower in Dicranopteris with high lignin content and lignin:N ratio than in Eucalyptus (Ma et al., 2009; Stewart et al., 2011). It was also supported by the higher decomposition constant of Eucalyptus than that of Dicranopteris. The litter decomposition constant of Eucalyptus in the control plots (0.56e0.59 yr-1) was similar to previous results from the close-by sites (0.51e0.77 yr1; Zhu et al., 2016). The litter decomposition constant of Dicranopteris in the control plots was 0.30e0.31 yr-1, which was also close to the result from the subtropics (0.25 yr-1; Ma et al., 2009). Furthermore, different species could make diverse responses to one disturbance (e.g., understory removal, Wright et al., 2015). Sun et al. (2017) reported that the survival of Castanopsis fissa seedlings in understory removal was significantly higher, while the Schima superba and Michelia macclurei seedlings were not sensitive to understory removal. Understory removal and tree removal could affect the litter quality (Henneron et al., 2018). However, in the present study, the initial leaf litter was exclusive of that from the understory/tree removal subplots. Therefore, the results could be limited to effects on the leaf litter from the control subplots. 5. Conclusion This study suggested that understory removal significantly reduced litter decomposition and litter C mineralization of Eucalyptus both in the 8- and 29-yr-old plantations, and significantly reduced N and P mineralization of Eucalyptus litter only in the 29-yr-old plantation. In contrast, it significantly decreased litter decomposition of Dicranopteris only in the 29-yr-old plantation, and did not affect C, N and P mineralization of Dicranopteris litter. Surprisingly, tree removal did not show any significant effect on litter decomposition and nutrient mineralization. Our results indicate that the effects of understory plants on leaf litter decomposition and nutrient mineralization is more significant than overstory trees, and it can be altered by stand age and plant species. These findings could promote the understanding of ecological processes of litter decomposition and nutrient mineralization in plantation forest ecosystems. Conflicts of interest The authors declare that they have no conflicts of interest. Acknowledgements This work was supported by the National Natural Science Foundation of China (41571249, 41771278, U1701246), the Hunan Provincial Natural Science Foundation of China (2017JJ3083), Science and Technology Program of Guangzhou, China (201707010344), Youth Innovation Promotion Association CAS, Open Foundation of the State Key Laboratory of Urban and Regional Ecology of China (SKLURE2016-2-5), and the Research Foundation of Education Bureau of Hunan Province, China (17B099). Special thanks to Mr. Mozheng Li, Shengxing Fu and Dr. Xiaomin Zhu for their helps in leaf litter collection and litterbags preparation. We are grateful to Dr. Arjun Pandey for editing the English language. References Aponte, C., García, L.V., Maranon, T., 2012. Tree species effect on litter decomposition and nutrient release in Mediterranean oak forests changes over time. Ecosystems 15, 1204e1218. Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol. Biochem. 35, 955e963. ssia Piccolo, M., Saint-Andre , L., Bouvet, J.M., Nouvellon, Y., de Moraes Gonçalves, J.L., Robin, A., Laclau, J.P., 2016. Bachega, L.R., Bouillet, J.P., de Ca Decomposition of Eucalyptus grandis and Acacia mangium leaves and fine roots in tropical conditions did not meet the Home Field Advantage hypothesis. For. Ecol. Manag. 359, 33e43. Bani, A., Pioli, S., Ventura, M., Panzacchi, P., Borruso, L., Tognetti, R., Tonon, G., Brusetti, L., 2018. The role of microbial community in the decomposition of leaf litter and deadwood. Appl. Soil Ecol. 126, 75e84. Bao, S., 2000. Analysis in Soil and Agrochemistry, third ed. Agricultural Press, Beijing. pp. 30e34, 42-49, 71-78. (In Chinese). Bonanomi, G., Cesarano, G., Gaglione, S.A., Ippolito, F., Sarker, T., Rao, M.A., 2017. Soil fertility promotes decomposition rate of nutrient poor, but not nutrient rich litter through nitrogen transfer. Plant Soil 412, 397e411. Bossio, D.A., Scow, K.M., 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb. Ecol. 35, 265e278.
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