Effects of various fertilization placements on the fate of urea-15N in moso bamboo forests

Forest Ecology and Management 453 (2019) 117632

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Effects of various fertilization placements on the fate of urea-15N in moso bamboo forests

T

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Wenhui Sua, Shaohui Fana, Jiancheng Zhaoa,b, , Chunju Caia a b

International Centre for Bamboo and Rattan, Key Laboratory of Bamboo and Rattan, Beijing 100102, China Zhejiang Academy of Forestry, Zhejiang Provincial Key Laboratory of Bamboo Research, Hangzhou, Zhejiang 310023, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Phyllostachys edulis 15 N-labeled urea N recovery efficiency Residual N N loss

Appropriate fertilization practice is crucial to increase nitrogen (N) recovery efficiency and decrease N loss. Our aim is to determine the appropriate fertilization placement and the target age in moso bamboo forests. A field experiment was conducted to determine the effects of application methods (furrow and hole) and depths (0–20 and 20–40 cm) on the fate of urea-15N in moso bamboo forests. The 15N tracer technique was used to investigate the fates of the applied 15N fertilizer. The largest biomass was obtained from the bamboo culm (42.25–54.09%), but the maximum absorption and N content occurred in the leaves (28.86–39.31%). The N recovery efficiency of urea-15N was significantly higher for deep applications (30.62–31.14%) than for shallow applications (26.68–27.49%), whereas no significant difference was found between the furrow and hole applications. The residual 15N was mainly concentrated in the fertilized soil layer, and the residual 15N recovered from the 0–60 cm soil layer was 16.29–19.47%. The highest N recovery efficiency (31.34%) and lowest N loss (49.91%) were observed for the furrow application at 20–40 cm. In addition, the N competitive ability and N recovery efficiency of the I du (moso bamboo age, 1–2 years old) bamboo were 0.069 mg kg−1 d−1 and 13.29%, respectively, which were significantly higher than those of the other ages. Therefore, furrow application at depth of 20–40 cm is recommended for practical applications, and the I du bamboo should be the target of fertilization in moso bamboo forests.

1. Introduction

the soil and the translocation of nutrient and photosynthesis products from the culms or leaves to the growing organs (Umemura and Takenaka, 2014). However, large amounts of nutrient are removed from bamboo forests every year due to the frequent timber and shoot harvests (Liu, 2009). In addition, the slow decomposition of the residual rhizome and stump after harvesting results in low nutrient return (Jiang, 2007). Therefore, high nutrient output and low nutrient input may cause an unsustainable level of long-term productivity in moso bamboo forests (Guan et al., 2017; Su, 2012). Studies have been conducted on the cycles of macronutrients in moso bamboo forests (Embaye et al., 2005; Umemura and Takenaka, 2014), and fertilization is the most direct and efficient method to improve stand productivity (Su, 2012). Nitrogen (N) is one of the most important macronutrients for moso bamboo, because it is the nutrient with the largest demand and greatest absorption in each growth period (Su, 2012). Therefore, nitrogenous fertilizers are essential to obtain good yields in moso bamboo forests (Su, 2012). However, excess N fertilizer and inappropriate application methods have led to low N recovery efficiency and high N losses

Bamboo is one of the most important forest resources, and it has a tree-like shape but belongs to the grass family (Jiang, 2007). Moso bamboo (Phyllostachys edulis (Carrière) J. Houz.) is one of the major giant bamboo species in China, which occupies > 4.43 million ha according to the 8th national forest inventory (National Forestry and Grassland Administration, 2014). This species is a versatile and rapidly renewable resource, providing a very high yield (culm and shoot) and good return on investment (Jiang, 2007). The culm can be harvested after four years and has been widely used as a major non-wood forest product and wood substitute for numerous purposes (Mertens et al., 2008; Song et al., 2011). Bamboo shoot is a traditional vegetable due to its high edible value, great taste, and high nutrition (Jiang, 2007; Zhao et al., 2018). Therefore, bamboo plays an increasingly important role in economic development (Zhao et al., 2019). Moso bamboo is characterized by its high growth rate during sprouting and its rapid biomass accumulation (Zhao et al., 2018). The rapid internode elongation is supported by the uptake of nutrient from

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Corresponding author at: Zhejiang Academy of Forestry, Zhejiang Provincial Key Laboratory of Bamboo Research, Hangzhou, Zhejiang 310023, China. E-mail address: [email protected] (J. Zhao).

https://doi.org/10.1016/j.foreco.2019.117632 Received 14 June 2019; Received in revised form 9 August 2019; Accepted 14 September 2019 Available online 18 October 2019 0378-1127/ © 2019 Elsevier B.V. All rights reserved.

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Kjeldahl’s method, Olsen’s extractable phosphorus method, and flame photometric method, respectively (Bao, 2005). This study was conducted in a moso bamboo forest with rich understory vegetation. Stem density management was conducted in parallel with the culm harvest in January 2015, but no fertilization management had been conducted. The understory species comprised Cyrtomium fortunei, Rhododendron maculiferum subsp. anhweiense, Mallotus apelta var. apelta, Rhus chinensis var. chinensis, Itea chinensis, Glochidion puberum, Rubus chingii, Dicranopteris dichotoma, Plantago depressa, Miscanthus floridulus, Galinsoga quadriradiata, Woodwardia japonica, and Boehmeria nivea var. nipononivea.

through ammonia (NH3) volatilization, runoff, leaching, and denitrification (Shi et al., 2012; Wallace et al., 2012; Chen et al., 2016). Previous study has shown that the input of urea in moso bamboo forests is > 500 kg ha−1, which far exceeds the demand for bamboo growth (Zhao, 2016). The uptake of broadcast-applied N fertilizer is relatively low in moso bamboo forests, and it has been shown that the N recovery efficiency was only 13.96% (Mao et al., 2016). Broadcast-applied N fertilizer remains near the soil surface and does not move into the root zone where it can be absorbed by moso bamboo (Chen et al., 2016). Efficient fertilizer applications are of great concern due to the close relationship with N recovery efficiency and environmental problems (Ju et al., 2009; Aikins et al., 2010; Guo et al., 2010; Reay et al., 2012; Su et al., 2015). The 4R Nutrient Stewardship is the foundation of best management practices for fertilizer, which comprehensively convey how fertilizer applications can be managed to achieve economic, social and environmental goals (IFA, 2009). Moreover, the efficient use of fertilizer depends on timing, rates, nutrient forms, and placement (Chen et al., 2016), which is the core of the 4R framework. Research has shown that the placement of fertilizer in the root zone may increase plant uptake and reduce nutrient loss (Murphy and Zaurov, 1994; Waddell and Weil, 2006). Rhizome roots and stump roots are the main absorbing organs for moso bamboo, which are usually located in the soil depth range of 10–30 cm (Jiang, 2007). Therefore, furrow application and hole application of fertilizer are commonly used in practice (Zhao et al., 2019). Recent studies on efficient fertilizer application in moso bamboo forests have mainly focused on N application rate and timing (Su, 2012), but few studies have been conducted on the appropriate placement. For efficient N utilization, the 15N tracer technique has been widely used to quantify the uptake, residual amounts, and loss of N fertilizer (Chen et al., 2016; Wang et al., 2016). However, little is known about the distribution and translocation of urea-15N in moso bamboo forest ecosystems. The objectives of this study were to (1) investigate the fates of the applied 15N fertilizer (15N-labeled urea) for different application methods and at different depths; and (2) determine the appropriate application placement in moso bamboo forests.

2.2. Experimental design The experiment was a factorial design with two fertilizer application methods (furrow and hole) and two application depths (0–20 and 20–40 cm). Fertilization treatments were applied as follows: F20 (furrow application, 0–20 cm), F40 (furrow application, 20–40 cm), H20 (hole application, 0–20 cm) and H40 (hole application, 20–40 cm). A control treatment with no fertilizer (Control) was also included. The experimental plot was 600 m2 (20 m × 30 m) with three replications. The distance between adjacent plots was > 20 m. Four trenches were excavated for isolation around the plots. The trench was 60 cm in depth and the rhizome was cut off, which could effectively prevent the longdistance transportation of nutrients. In order to maintain a consistent stand structure, density structure and age structure adaptations were conducted by logging. The diameter at breast height (DBH, 1.3 m) and age of all bamboos in each plot were recorded. Because of the unique growth characteristic of moso bamboo forests with a vegetative cycle of two years (on-year and off-year), the age was expressed as “du” (Tang et al., 2016). One (I) “du” represents 1–2 years, and similarly, 2 (II) and 3 (III) “du” correspond to 3–4 and 5–6 years, respectively (Tang et al., 2016). The descriptions of the stand characteristics are shown in Table 2. According to the previous research, 242 kg ha−1 of urea (46% N), 178 kg ha−1 of calcium superphosphate (12% P2O5) and 147 kg ha−1 of potash chloride (59% K2O) were applied once to the experiment fields (Su, 2012). Moreover, 250 g of 15N-labeled urea (10.18 at%, provided by the Shanghai Research Institute of Chemical Industry) was applied in each of the fertilization plots. All fertilizers were mixed and blended evenly before application, and then applied at the designed depth. First, pre-mix 250 g of 15N-labeled urea and 2 kg of urea evenly, then spread 12.52 kg urea evenly into a certain thickness, sprinkle 2.25 kg mixed urea evenly on its surface, then turned over and mixed evenly. After this process, the mixture of urea, calcium superphosphate and potash chloride was mixed evenly. For the furrow application, each plot consisted of 9 fertilizer furrows (0.1 m in width and 2 m apart) along the contour. For the hole application, the fertilizers were applied in a one-fourth annular groove (30 cm internal diameter, 40 cm external diameter). The fertilizers were applied in June 2015 (off-year), which was during the maximum period of nutrient demand. After fertilization, the original soil was backfilled.

2. Material and methods 2.1. Site description The field experiment was conducted in Huangshan county in Anhui province, China (118°32′E, 32°12′N). The region is characterized by a humid mid-subtropical monsoon climate with an annual average temperature of 15.3 °C and an annual mean precipitation of 1500 mm. The mean annual sunshine duration is 1752.7 h and the mean relative humidity is > 80%. The experimental site has an altitude of 492 m above sea level and a slope of 27°. According to the USDA soil classification, the soils at the experimental site are Ultisols. Before fertilization, the soil was sampled at depth of 0–60 cm. The physical and chemical properties of the soil were presented in Table 1. Soil pH was measured in a 1:2.5 (m/v) soil/water suspension. Soil organic matter was analyzed using the H2SO4-K2Cr2O7 wet oxidation method (Fan et al., 2016). Soil total N, total P and total K were determined using the

2.3. Plant and soil sampling and analyses For each age (du), one bamboo stand with an average DBH was selected and harvested in each plot in January 2016. The bamboo plants were separated into leaves, branches, culms, stump, and stump roots. Rhizomes and rhizome roots were sampled from three random micro-plots (1 m × 1 m) in each plot. After washing away the soil and impurities, the fresh weight of each organ was weighed and sampled. The fresh samples were dried at 70 °C to constant weight for the determination of the dry weight, and the biomass of each organ was calculated. The dry samples were milled and sieved through a 0.15 mm screen for 15N analysis. The soil was sampled in parallel with the moso bamboo. The soil

Table 1 Physical and chemical properties of soil profiles in the experimental site. Soil depth/(cm)

0–20

20–40

40–60

Bulk density/(g cm−3) pH/(1:2.5) Organic matter/(g kg−1) Total N/(g kg−1) Total P/(g kg−1) Total K/(g kg−1)

1.07 ± 0.14 4.92 ± 0.09 31.19 ± 1.89 1.72 ± 0.16 0.47 ± 0.09 16.34 ± 1.46

1.21 ± 0.12 4.78 ± 0.08 23.16 ± 1.36 1.65 ± 0.21 0.32 ± 0.07 14.03 ± 1.32

1.32 ± 0.13 4.73 ± 0.07 15.37 ± 1.99 0.98 ± 0.12 0.25 ± 0.06 13.19 ± 1.27

The values are the means ± standard deviations (SD). 2

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Table 2 Characteristics of the four experimental stands. Treatment

Density/(individual ha−1)

Mean DBH/(cm)

Mean Height/(m)

Age Structure/(I:II:III)

Control F20 F40 H20 H40

1533 1433 1600 1544 1533

10.96 11.29 10.99 11.17 10.65

15.50 15.42 14.11 13.94 14.96

0.53:0.32:0.15 0.56:0.30:0.14 0.56:0.29:0.15 0.55:0.28:0.17 0.51:0.32:0.17

± ± ± ± ±

88 58 120 117 88

± ± ± ± ±

1.41 1.52 1.32 1.33 1.28

± ± ± ± ±

1.49 1.54 0.98 1.94 1.46

The values are the means ± standard deviations (SD). Control, F20, F40, H20, and H40 represent no fertilization, furrow application in 0–20 and 20–40 cm and hole application in 0–20 and 20–40 cm, respectively. Age structure represents the proportion of individuals of three ages. I, II and III represent 1–2, 3–4, and 5–6 years, respectively. Table 3 Effects of various fertilization placements on biomass in moso bamboo forests. Treatment

Age

Dry matter (t ha−1) Leaf

F20

F40

H20

H40

I II III I II III I II III I II III

1.59 0.95 0.38 3.67 1.69 0.72 1.73 0.93 0.44 1.59 0.99 0.62

Branch ± ± ± ± ± ± ± ± ± ± ± ±

0.16Ab 0.08Bb 0.05Cb 0.41Aa 0.20Ba 0.11Ca 0.23Ab 0.13Bb 0.06Cb 0.19Ab 0.14Bb 0.09Ca

2.34 1.44 0.53 3.23 1.67 1.12 2.42 1.81 0.90 2.76 1.67 0.76

± ± ± ± ± ± ± ± ± ± ± ±

0.25Ab 0.18Ba 0.06Cc 0.48Aa 0.19Ba 0.10Ba 0.36Ab 0.25Ba 0.07Cb 0.31Aa 0.23Ba 0.09Cb

Culm

Stump

15.58 ± 1.75Aa 8.37 ± 1.02Ba 4.66 ± 0.59Ca 16.72 ± 1.96Aa 9.05 ± 1.32Ba 4.53 ± 0.67Ca 18.52 ± 1.91Aa 8.77 ± 0.97Ba 5.26 ± 0.63Ca 10.21 ± 1.12Ab 8.16 ± 0.94Aa 3.23 ± 0.46Bb

2.41 1.56 0.50 2.41 0.96 0.62 2.37 1.63 0.51 2.55 1.37 0.65

± ± ± ± ± ± ± ± ± ± ± ±

0.32Aa 0.16Ba 0.08Cb 0.39Aa 0.12Bb 0.07Ba 0.27Aa 0.36Ba 0.06Cb 0.32Aa 0.15Ba 0.09Ca

Stump root

Rhizome

Rhizome root

2.66 1.78 0.57 1.65 0.79 0.43 1.51 1.33 0.97 2.48 1.18 0.42

6.83 ± 0.86c

2.93 ± 0.35c

9.48 ± 1.03a

2.33 ± 0.30d

7.99 ± 0.71b

3.07 ± 0.39b

8.22 ± 0.93b

4.02 ± 0.48a

± ± ± ± ± ± ± ± ± ± ± ±

0.31Aa 0.20Ba 0.07Cb 0.14Ab 0.10Bc 0.06Bb 0.19Ab 0.16Bb 0.11Ca 0.31Aa 0.15Bb 0.05Cb

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level.

samples were collected from the 0–60 cm soil layer and separated into 20–cm depth increments. The soil samples were obtained at three random sites in the unfertilized plots and three fertilization furrows (holes) in the fertilized plots. The samples taken from the same depth segments in each plot were mixed to represent a single sample. All soil samples were dried at room temperature and sieved through a 0.15 mm screen prior to 15N analysis. The total N of all plant and soil samples, the natural abundance of plant and soil in the unfertilized plot, and the at% 15N in the fertilized plot were determined using an Isotope Ratio Mass Spectrometer (Thermo Finnigan MAT DELTA plus XP, Germany) at the Institute of Botany of the Chinese Academy of Sciences.

Residual 15N in soil(kg ha −1) = (fertilization area(m2) × soil thickness(cm) × soil bulk density(g cm−3) × N concentration(g kg−1) × Ndff soil × 10−2) /Plot area(m2) Fertilizer 15N loss(kg ha −1) = Total fertilizer 15N(kg ha −1) - (4) − (5) (6)

N recovery efficiency(%) = (4)/Total

fertilizer 15N(kg

ha−1)

× 100

N residual efficiency(%) = (5)/Total fertilizer 15N(kg ha−1) × 100 N loss efficiency(%) = (6)/Total fertilizer 15N(kg ha −1) × 100

2.4. Calculation methods The percentage of 15N derived from urea-15N (Ndff, %) was calculated by the following equations (Shi et al., 2012; Chen et al., 2016):

Ndff(%) =

(5)

b−a × 100 c−a

2.5. Statistical analysis One-way analysis of variance (ANOVA) was used to determine the significant differences between treatments for each variable over the whole experiment. Means were separated by Duncan’s multiple range test and statistical significance was evaluated at P < 0.05. All statistical analyses were conducted in SAS 9.0 software (SAS Institute, 2001). The figures were prepared using the Origin 8.6 software (OriginLab Corporation, 2015).

(1)

where a is the at% 15N in the unfertilized plant organ or soil, b is the at % 15N in the fertilized plant organ or soil, and c is the at% 15N in the fertilizer.

Organ total N(kg ha−1) = organ dry matter(kg ha−1) × N concentration(g kg−1) × 10−3

3. Results (2) 3.1. Moso bamboo biomass

Organ 15N from fertilizer(kg ha −1) = (2) × Ndff organ × 10−2 Plant 15N from fertilizer(kg ha−1) =

∑ (organ 15N from fertilizer)

(3)

The application method and depth significantly affected the biomass of moso bamboo forests (Table 3). For all fertilization treatments, the dry matter of all organs (except rhizome and rhizome root) of I du was significantly higher than that of II and III du (P < 0.05). The culm

(4) 3

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Table 4 Effects of various fertilization placements on N concentration in moso bamboo forests. Treatment

Age

N concentration (g kg−1) Leaf

F20

F40

H20

H40

I II III I II III I II III I II III

32.81 31.79 32.40 31.84 33.75 32.48 32.29 30.61 31.76 32.25 31.29 32.52

Branch ± ± ± ± ± ± ± ± ± ± ± ±

4.21Aa 3.42Aa 3.69Aa 3.52Aa 3.64Aa 4.31Aa 3.12Aa 2.90Aa 2.62Aa 3.45Aa 3.19Aa 4.01Aa

5.87 5.93 5.82 5.53 6.09 5.90 5.62 5.36 6.20 5.69 5.66 5.28

± ± ± ± ± ± ± ± ± ± ± ±

Culm 0.62Aa 0.53Aa 0.60Aa 0.55Aa 0.51Aa 0.62Aa 0.61Aa 0.57Aa 0.53Aa 0.62Aa 0.57Aa 0.50Aa

1.55 2.45 2.02 2.64 2.77 2.36 2.62 2.81 2.44 3.50 2.80 3.20

± ± ± ± ± ± ± ± ± ± ± ±

0.18Cc 0.23Aa 0.24Bb 0.30Ab 0.29Aa 0.28Ab 0.23Ab 0.31Aa 0.19Ab 0.41Aa 0.23Aa 0.27Aa

Stump

Stump root

Rhizome

Rhizome root

12.21 ± 1.02Ab 5.84 ± 0.63Bc 8.12 ± 0.92Bb 8.86 ± 0.71Ac 9.80 ± 1.03Aa 9.93 ± 0.82Aa 15.32 ± 1.43Aa 7.60 ± 0.83Bb 8.45 ± 0.76Bb 8.21 ± 0.71Ac 4.85 ± 0.52Bc 6.78 ± 0.81Ac

6.82 5.72 4.79 7.52 7.66 6.70 7.65 5.12 5.39 7.40 5.60 5.20

7.30 ± 0.83b

6.85 ± 0.92a

11.95 ± 1.09a

7.95 ± 0.98a

7.48 ± 0.66b

5.18 ± 0.72b

8.35 ± 0.97b

6.71 ± 0.69a

± ± ± ± ± ± ± ± ± ± ± ±

0.72Aa 0.51Bb 0.56Cc 0.93Aa 0.86Aa 0.73Aa 0.91Aa 0.42Bb 0.46Bb 0.90Aa 0.46Bb 0.63Bb

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level.

the bamboo age. The total N uptake of the I du bamboo was the highest due to its high biomass and was significantly higher than that of the II and III du bamboo (P < 0.05). The total N uptake was the highest for the bamboo leaf, and was significantly higher than that of the other organs, accounting for an average of 31.23% (ranging from 28.86% to 39.31%) of total N uptake. The total N uptake of the aboveground parts was higher than that of the underground parts (P < 0.05). Treatment F40 had the highest total N uptake of 501.77 kg ha−1.

biomass was significantly higher than that of other organs, accounting for an average of 49.53% (ranging from 42.45% to 54.09%) of the total biomass. The rhizomes had the second largest proportion of biomass in the bamboo forest at 6.83, 9.48, 7.99, and 8.22 t ha−1 for the F20, F40, H20, and H40 treatments, respectively. The underground biomass (including stump, stump root, rhizome, and rhizome root) of the moso bamboo forest was similar for all treatments, and the aboveground biomass (including leaf, branch and culm) was higher than the underground biomass. The biomass of the rhizome-root system (rhizome and rhizome root) was in the range of 9.76–12.24 t ha−1, accounting for 17.71–24.06% of the total biomass. The highest biomass of the rhizome-root system was 12.24 t ha−1 for the H40 treatment.

3.3. Distribution of urea-15N in moso bamboo forests The application method and depth significantly affected Ndff in moso bamboo forests (Table 6). Significant differences in the Ndff were found between different organs. The average Ndff in the stump (0.23%) and stump root (0.19%) were higher than the values of the other organs. The average Ndff in the branch (0.12%) and culm (0.12%) were roughly the same, and the difference was not significant (P > 0.05). The application depth significantly affected the total 15N uptake in moso bamboo forests (Table 7). The total 15N uptake was significantly higher at fertilization depth of 20–40 cm than at 0–20 cm (P < 0.05). However, no significant difference was found between the furrow application and hole application at the same fertilization depth (P > 0.05). With the increase of bamboo age, the 15N uptake in the leaf, branch, stump, and stump root showed a decreasing trend. In all treatments, the 15N uptake in the leaf was significantly higher than that of the other organs (P < 0.05). The leaf 15N uptake was in the range of 26.90–37.21% (mean 30.80%). The 15N uptake in the leaf at different

3.2. N Concentration and N uptake The N concentrations differed for the different organs (Table 4). The N concentration was significantly higher in the leaves than in the other organs. For each treatment, no significant difference was found in the N concentration in the leaves and branches among the three different ages (P > 0.05). Additionally, for each age, no significant difference was found in the N concentration in leaves and branches among the four fertilization treatments (P > 0.05). The highest total N concentrations in rhizome and rhizome root were observed in F40 at 11.95 and 7.95 g kg−1, respectively. The application method and depth significantly affected the total N uptake in moso bamboo forests (Table 5). The total N uptake in each organ (except rhizome and rhizome root) decreased with the increase of Table 5 Effects of various fertilization placements on N uptake in moso bamboo forests. Treatment

F20

F40

H20

H40

Age

I II III I II III I II III I II III

Total N uptake (kg ha−1) Leaf

Branch

Culm

Stump

Stump root

Rhizome

Rhizome root

52.20 ± 4.95Ab 30.28 ± 3.24Bb 12.28 ± 1.04Cb 116.72 ± 10.34Aa 56.98 ± 6.98Ba 23.54 ± 2.64Ca 55.95 ± 6.45Ab 28.48 ± 3.01Bb 14.07 ± 1.23Cb 51.28 ± 5.75Ab 30.95 ± 3.68Bb 20.30 ± 2.72Ca

13.73 ± 1.24Ab 8.56 ± 0.93Ba 3.07 ± 0.24Cb 17.83 ± 1.35Aa 10.19 ± 1.03Ba 6.62 ± 0.75Ca 13.60 ± 1.42Ab 9.73 ± 1.01Ba 5.60 ± 0.73Ca 15.70 ± 1.63Aa 9.43 ± 0.82Ba 4.04 ± 0.39Cb

24.10 ± 2.64Ac 20.53 ± 2.31Aa 9.41 ± 0.82Bc 44.11 ± 4.93Aa 25.06 ± 2.34Ba 10.67 ± 1.20Cb 48.62 ± 5.42Aa 24.67 ± 3.21Ba 12.82 ± 1.34Ca 35.69 ± 4.75Ab 22.87 ± 2.45Ba 10.33 ± 1.03Cb

29.47 ± 2.54Aa 9.10 ± 1.03Bb 4.04 ± 0.52Cb 21.39 ± 2.36Ab 9.38 ± 0.97Bb 6.18 ± 0.75Ba 36.36 ± 4.37Aa 12.38 ± 1.34Ba 4.30 ± 0.39Cb 20.89 ± 2.31Ab 6.66 ± 0.72Bc 4.39 ± 0.65Bb

18.12 ± 2.14Aa 10.20 ± 1.24Ba 2.72 ± 0.32Cb 12.37 ± 1.01Ab 6.06 ± 0.56Bb 2.89 ± 0.29Cb 11.59 ± 1.03Ab 6.82 ± 0.80Bb 5.21 ± 0.62Ba 18.34 ± 1.34Aa 6.60 ± 0.59Bb 2.19 ± 0.23Cb

49.81 ± 5.71c

20.08 ± 2.57b

113.26 ± 10.23a

18.52 ± 2.11b

59.78 ± 6.98b

15.92 ± 1.50c

68.68 ± 6.41b

26.98 ± 2.43a

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level. 4

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Table 6 Effects of various fertilization placements on Ndff in moso bamboo forests. Treatment

Age

Ndff (%) Leaf

F20

F40

H20

H40

I II III I II III I II III I II III

0.19 0.17 0.11 0.13 0.12 0.07 0.16 0.18 0.14 0.16 0.16 0.17

Branch ± ± ± ± ± ± ± ± ± ± ± ±

0.02Aa 0.02Aa 0.01Bb 0.01Ac 0.01Ab 0.01Bc 0.02Bb 0.02Aa 0.01Cb 0.01Ab 0.01Aa 0.02Aa

0.16 0.14 0.15 0.11 0.10 0.06 0.12 0.12 0.09 0.13 0.12 0.13

± ± ± ± ± ± ± ± ± ± ± ±

Culm 0.02Aa 0.01Aa 0.01Aa 0.01Ab 0.01Ac 0.01Bb 0.01Ab 0.01Ab 0.01Bb 0.01Ab 0.01Ab 0.02Aa

0.11 0.15 0.12 0.10 0.09 0.07 0.10 0.14 0.08 0.13 0.14 0.14

Stump ± ± ± ± ± ± ± ± ± ± ± ±

0.01Ab 0.01Aa 0.01Aa 0.01Ac 0.01Ab 0.01Ab 0.01Bc 0.01Aa 0.01Bb 0.01Aa 0.02Aa 0.02Aa

0.28 0.18 0.26 0.24 0.21 0.18 0.25 0.17 0.16 0.26 0.25 0.28

± ± ± ± ± ± ± ± ± ± ± ±

0.03Aa 0.02Bc 0.03Aa 0.03Aa 0.02Bb 0.01Cb 0.02Aa 0.02Bc 0.02Bb 0.03Aa 0.03Aa 0.02Aa

Stump root

Rhizome

Rhizome root

0.16 0.15 0.17 0.17 0.17 0.14 0.20 0.13 0.11 0.31 0.22 0.29

0.19 ± 0.02a

0.16 ± 0.01a

0.12 ± 0.01b

0.17 ± 0.02a

0.12 ± 0.01b

0.15 ± 0.01a

0.18 ± 0.02a

0.14 ± 0.01a

± ± ± ± ± ± ± ± ± ± ± ±

0.02Ab 0.01Ab 0.01Ab 0.01Ab 0.02Ab 0.01Ac 0.02Ab 0.01Bb 0.01Bc 0.03Aa 0.02Ca 0.03Ba

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level. 0.10

ages was consistent with the total 15N uptake of moso bamboo forests. The 15N uptake of the III du bamboo was the lowest, and it was significantly lower than that of I du bamboo (P < 0.05). With the increase of bamboo age, the absorption efficiency decreased gradually (Fig. 1). The absorption efficiency of the I du bamboo was significantly higher than that of the II and III du bamboo (P < 0.05). However, no significant difference was found between the absorption efficiencies of the II and III du bamboo (P > 0.05).

Absorption efficiency (mg kg-1 d-1)

0.08

3.4. Distribution of residual urea-15N in soil At the end of our experiment, the total residual urea-15N for the furrow treatments were 328.37 and 381.39 g ha−1 at the application depths of 0–20 and 20–40 cm, respectively, and the corresponding values for the hole treatment were 339.71 and 392.49 g ha−1, respectively (Fig. 2). For the same application method, significant differences were found in the total residual urea-15N between the fertilization depths of 0–20 and 20–40 cm in each soil layer (P < 0.05). For the 0–20 cm application, the residual urea-15N decreased with the increase of soil depth. Most residual urea-15N remained in the 0–20 cm soil layer, accounting for 61.86% of the total residual urea-15N for the furrow application (F20) and 62.22% for the hole application (H20). However, for the 20–40 cm application, most residual urea-15N remained in the 20–40 cm soil layer, accounting for 68.06% of the total residual urea-15N for the furrow application (F40) and 64.83% for the hole application (H40). Additionally, the residual urea-15N in the 40–60 cm soil layer for the H40 and F40 treatments was significantly higher than Table 7 Effects of various fertilization placements on Treatment

F20

F40

H20

H40

Age

I II III I II III I II III I II III

15

N uptake (g ha

−1

15

a

b 0.06

b

0.04

0.02

0.00 I

II

III

Age (du)

Fig. 1. Total absorption efficiency of different ages in moso bamboo forests. The error bars indicate the stand deviation (SD). Different lowercase letters indicate significant differences among different ages at the P < 0.05 level.

that in the 0–20 cm soil layer, respectively (P < 0.05). The residual urea-15N in the 20–40 cm soil layer for the furrow treatment at the application depths of 0–20 and 20–40 cm were 78.25 and 259.56 g ha−1, respectively, and were higher than the corresponding values of 72.30 and 254.47 g ha−1 for the hole treatment.

N derived from urea-15N in moso bamboo forests.

)

Leaf

Branch

Culm

Stump

Stump root

Rhizome

Rhizome root

96.96 ± 11.32Ab 51.52 ± 6.21Bb 14.03 ± 1.95Cb 150.61 ± 13.69Aa 67.19 ± 7.32Ba 15.79 ± 2.06Cb 89.65 ± 8.01Ab 51.40 ± 4.96Bb 19.13 ± 2.34Cb 81.62 ± 9.16Ab 50.22 ± 5.67Bb 34.22 ± 4.34Ca

22.59 ± 2.56Aa 11.81 ± 1.35Ba 4.54 ± 5.04Ca 19.43 ± 2.64Ab 10.54 ± 1.34Ba 4.20 ± 3.61Ca 16.07 ± 1.95Ac 11.88 ± 1.34Ba 4.93 ± 0.41Ca 20.34 ± 1.83Ab 11.34 ± 1.51Ba 5.20 ± 0.46Ca

26.88 ± 3.12Ab 29.87 ± 3.01Ab 11.56 ± 1.31Bb 42.36 ± 5.14Aa 23.16 ± 3.21Bc 7.80 ± 0.71Cd 50.08 ± 5.34Aa 34.95 ± 3.69Ba 10.34 ± 1.02Cc 47.97 ± 4.32Aa 32.77 ± 3.54Ba 13.95 ± 1.75Ca

82.51 ± 9.65Aa 16.24 ± 1.97Ba 10.65 ± 1.35Ba 50.85 ± 5.34Ab 19.87 ± 2.25Ba 11.01 ± 1.36Ca 89.74 ± 7.69Aa 20.70 ± 2.65Ba 6.98 ± 0.89Cb 53.63 ± 7.01Ab 16.32 ± 1.95Ba 12.38 ± 1.53Ba

29.78 ± 2.63Ab 15.09 ± 1.64Ba 4.66 ± 0.53Cc 20.88 ± 2.16Ac 10.29 ± 1.32Bb 3.92 ± 0.46Cd 23.44 ± 2.65Ac 8.89 ± 1.02Bb 5.65 ± 0.67Bb 56.06 ± 6.32Aa 14.73 ± 1.82Ba 6.35 ± 0.59Ca

94.00 ± 8.54b

31.51 ± 2.65b

139.26 ± 16.32a

30.57 ± 3.45b

69.74 ± 8.65c

24.27 ± 2.69c

122.09 ± 11.75a

38.15 ± 4.87a

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level. 5

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W. Su, et al.

Urea-15N residual (g ha-1)

Soil layer (cm)

0-20

50

100

150

200

250

Urea-15N residual (g ha-1)

300

0

a b

a

150

200

250

300

a

a

20-40

b

a

40-60

F20 F40

b

100

b

0-20

a

20-40

40-60

50

b

Soil layer (cm)

0

H20 H40

b

Fig. 2. The distribution of residual urea-15N in the soil. The error bars indicate the stand deviation (SD). Different lowercase letters of the same soil layer indicate significant differences among different treatments at the P < 0.05 level.

3.5. Fate of urea-15N in bamboo-soil system

18

The application method had no effect on the N recovery efficiency at the same fertilization depth, whereas the fertilization depth had a significant effect on the N recovery efficiency for the same application method (Table 8). The N recovery efficiency in the leaves was in the range of 7.94–11.59%, which was much higher than that of the other organs. The N recovery efficiency was lower in the branch and rhizome root than in the other organs. With increasing bamboo age, the N recovery efficiency decreased, and the N recovery efficiency of the I du bamboo was significantly higher than that of the II and III du bamboo (P < 0.05, Fig. 3). The recovered urea-15N in the moso bamboo forests increased with increasing application depth, and it was significantly higher for deeper applications (H40 and F40) than for shallower applications (H20 and F20) (P < 0.05). However, the opposite result was observed for the N loss (Fig. 4). The N loss decreased with the increase of application depth, and it was significantly higher in the H20 and F20 treatments than in the H40 and F40 treatments (P < 0.05). The residual urea-15N in the soil was in the range of 16.29–19.47% for all treatments; these values were much lower than the N recovery efficiency and N loss. The residual N was significantly higher for deep fertilization than for shallow fertilization (P < 0.05). However, no significant difference was found in the residual urea-15N between F20 and H20 (P > 0.05). In the F20 and H20 treatments, the N loss ratio was higher than the sum of the N recovery efficiency and residual N ratio, respectively. In all fertilization treatments, the F40 treatment had the highest N recovery efficiency and residual N and the lowest N loss.

15

Treatment

F20 F40 H20 H40

15

a

N recovery efficiency (%)

III

a

a

12

9

b

b

b

b

6

c c

3

c

c

0 F20

F40

H20

H40

Treatment

Fig. 3. Effects of various fertilization placements on the N recovery efficiency of different ages in moso bamboo forests.The error bars indicate the stand deviation (SD). Different lowercase letters of the same treatment indicate significant differences among different ages at the P < 0.05 level.

by using labeled 15N-fertilizer (Harmsen and Moraghan, 1988; Cassman et al., 2002). The 15N-labeled method is well suited for studies on N fertilizer use efficiency and N balance in moso bamboo forest ecosystems. In our study, we applied the 15N-labeled method to quantify the fates of the applied N fertilizer (15N-labeled urea) in the bamboo-soil system, and to determine the appropriate application placement in moso bamboo forests. In the present research, the biomass of all organs (except for the rhizome and rhizome root) was the highest of I du bamboo due to the age structure, which accounted for more than half of the total bamboo

The N fertilizer applied to the soil had three fates, namely: uptake by moso bamboo, remaining in the soil, or loss from the bamboo-soil system (Shi et al., 2012). N fertilizer recovery can be directly measured

15

II

a

4. Discussion

Table 8 Effects of various fertilization placements on

I

N recovery efficiency in moso bamboo forests.

N recovery efficiency (%)

Leaf

Branch

8.06 ± 0.95b 11.59 ± 1.36a 7.94 ± 0.93b 8.24 ± 0.80b

1.93 1.69 1.63 1.83

± ± ± ±

Culm 0.26a 0.21b 0.19b 0.28a

3.39 3.64 4.73 4.70

Stump ± ± ± ±

0.46b 0.40b 0.53a 0.55a

5.43 4.05 5.82 4.08

± ± ± ±

0.72a 0.53b 0.86a 0.49b

Stump root

Rhizome

Rhizome root

Total

2.46 1.74 1.88 3.83

4.66 6.91 3.46 6.05

1.56 1.52 1.22 1.89

27.49 31.14 26.68 30.62

± ± ± ±

0.32b 0.21c 0.19c 0.43a

± ± ± ±

0.59b 0.72a 0.41c 0.63a

± ± ± ±

0.18b 0.20b 0.11c 0.24a

± ± ± ±

2.49b 2.69a 2.42b 2.73a

Different capital letters of the same treatment in the same column indicate significant differences among different ages at the P < 0.05 level, and different lowercase letters of the same age in the same column indicate significant differences among different treatments at the P < 0.05 level. 6

Forest Ecology and Management 453 (2019) 117632

W. Su, et al. 120 N loss efficiency

N residual efficiency

upper soil layer, resulting in less N infiltrating into the deep soil layer. In contrast, NH4+-N may be immobilized by the soil at 0–20 cm during NH3 volatilization when the N fertilizer was applied at 20–40 cm soil depth. The N recovery efficiency of treatments F40 and H40 were significantly higher than those of treatments F20 and H20, but the N loss exhibited the opposite trend. This indicated that the N recovery efficiency significantly increased with the increase of fertilization depth, whereas the N losses decreased. Similar results were reported by Ding et al (2015). In this study, the average N recovery efficiency was relatively low at 28.98%, but it was significantly higher than the previous study by Mao (2015), who found that the N recovery efficiency was 13.96% in moso bamboo forests after broadcast application. The surface-applied N fertilizer remains near the soil surface and cannot move into the root zone where it can be absorbed by the moso bamboo. The potential N loss (average of 53.14% among all treatments) was higher than reported previously. Mao (2015)reported 45.15% of N loss in moso bamboo forests. It is well known that NH3 volatilization, nitrification–denitrification, runoff, and leaching are the main pathways of N loss (Lin et al., 2007; Das et al., 2009; Zhao et al., 2016). In addition, deep placement of N fertilizer results in considerably less NH3 volatilization than surface applications (Zaman and Blennerhassett, 2010; Liu et al., 2015). Therefore, the higher potential N loss in this study may be the result of higher nitrification–denitrification, runoff, and leaching losses. In our study, the N recovery efficiency of the I du bamboo was significantly higher than that of the II and III du bamboo, which was consistent with the results of a previous study by Mao (2015). Although the N recovery efficiency of the I du bamboo was the highest, it did not accurately explain the difference in N absorption and utilization of bamboo plants due to the different biomass quantities of bamboo in different ages. Therefore, the absorption efficiency (15N uptake per unit time and biomass) was used to describe the N competitive ability. With the increase of bamboo age, the absorption efficiency decreased gradually, suggesting that the key target of fertilization in moso bamboo forests was the I du bamboo. As a clonal plant, moso bamboo is able to transport resources between the ramets of the clonal plants through the bamboo rhizome. The existence of physiological integration is an open question, and its effect on the N utilization mechanism remains unclear. Although the N competitive ability and N recovery efficiency of the I du bamboo were the highest, it is uncertain whether the absorbed N of the I du bamboo originated from the bamboos of the other ages. Therefore, further research on N physiological integration should be conducted to explore the mechanisms of high N recovery efficiency in moso bamboo forests.

N recovery efficiency

100

Percentage(%)

80

60

40

20

0 F20

F40

H20

H40

Treatment Fig. 4. Effects of various fertilization placements on the fate of urea-15N in moso bamboo forests.

biomass (Table 1). The bamboo culm had the largest biomass. This is consistent with the results of a previous study, which found that the proportion of bamboo culm to total biomass was 80.63% (Tian, 2011). The N concentration and the N uptake was the highest for the leaves, which may be related to photosynthesis. Additionally, the total N uptake of the I du bamboo was significantly higher than that of the other ages, suggesting that the leaves of the I du bamboo exhibited strong photosynthetic capacity. A similar trend was also observed by Gao (2013, 2014), who found that the photosynthetic rate of the I and II du bamboo leaves increased significantly after the application of N fertilizer. Although the biomass was largest for the bamboo culm, its N uptake was low due to the low N concentrations. The N application placement affected the distribution of 15N in moso bamboo forests. Previous research has reported that 50.11–62.59% of the total 15N uptake was partitioned to the stump and 8.35–9.98% was concentrated in the leaves (Cheng et al., 2017). In our study, 26.90–37.21% of the total 15N uptake was partitioned to the leaves. The difference in results may be attributed to the fertilization method. In the previous study, the cavity injection fertilization method was used to induce N loss. The 15N-labeled urea was injected into the junction of the culm base and bamboo stump, resulting in the accumulation of 15N in the bamboo stump (Cheng et al., 2017). However, in this study, urea-15N was applied to the root zone by furrow application or hole application, which may stimulate root uptake and transport to the leaves. The 15N concentration in the soil layer was used to investigate the residual amount and downward movement of the N fertilizer. The application method did not affect the total amount of residual 15N in the 0–60 cm soil layer. On average, the residual amount of 15N-labelled urea in the 0–60 cm soil layer was 360.49 g ha−1, accounting for 17.88% of the total 15N application. However, the total residual amount of 15N-labelled urea was significantly higher at the fertilization depth of 20–40 cm than at 0–20 cm. The higher residual 15N at the fertilization depth of 20–40 cm may be attributed to less N loss through NH3 volatilization (Zhao et al., 2016). In our study, the residual 15N was mainly concentrated in the fertilized soil layer, which was related to N immobilization in the soil organic matter (Garabet et al., 1998; Giacomini et al., 2010). This result is inconsistent with some previous reports, which showed that the residual 15N decreased with the increase of soil layer (Chen et al., 2016; Mao, 2015; Shi et al., 2012; Wang et al., 2016). The differences in the results may be attributed to the fertilization placement. When the N fertilizer was applied under the soil surface (0–20 cm), more available N was immobilized by the microbes in the

5. Conclusion This study clearly demonstrated that the fate and proportion of 15Nlabelled urea were significantly influenced by the fertilizer application method and depth in moso bamboo forests. For the same application method, the N recovery efficiency increased and N loss decreased with the increase of the fertilization depth. However, no significant differences were found between the furrow application and hole application for the same application depth. Although the bamboo culm had the largest biomass among all organs, the maximum absorption and largest N content occurred in the leaves. The residual 15N was mainly concentrated in the fertilized soil layer. The N competitive ability and N recovery efficiency were the highest for the I du bamboo. The results indicated that, furrow application at depth of 20–40 cm should be recognized as appropriate application placement, and the I du bamboo should be the key target of fertilization in moso bamboo forests. However, it is uncertain whether the absorbed N of the I du bamboo was originated from the bamboos of the other ages due to the physiological integration. Therefore, further research on the N physiological integration should be conducted to explore the mechanisms of high N 7

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recovery efficiency in moso bamboo forests.

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