Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China

Ecological Engineering 86 (2016) 174–182

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Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China Wen Yang a,b , Shuqing An a,b,∗ , Hui Zhao a,b , Lingqian Xu a,b , Yajun Qiao a,b , Xiaoli Cheng c,∗∗ a

School of Life Science and Institute of Wetland Ecology, Nanjing University, Nanjing 210093, PR China Jiangsu Engineering Laboratory of Wetland Restoration, Changshu 215500, PR China c Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, PR China b

a r t i c l e

i n f o

Article history: Received 12 January 2015 Received in revised form 12 October 2015 Accepted 10 November 2015 Keywords: Coastal wetlands Light fraction Mineral-associated organic matter Soil organic C and N Particulate organic matter Soil density and size fractionation

a b s t r a c t Plant invasion may impact ecosystem structure and function, and further affect soil organic matter (SOM) dynamics. However, the influence of plant invasion on soil organic carbon (C) and nitrogen (N) pools sizes, stability, and turnover in SOM of invaded ecosystems is not fully understood. In this study, soil C and N contents, and ␦13 C and ␦15 N values of free light fraction (LF), intra-aggregate particulate organic matter (iPOM) and mineral-associated organic matter (mSOM) were investigated in an invasive Spartina alterniflora community, adjacent bare flat and native Suaeda salsa and Phragmites australis communities. Short-term S. alterniflora invasion significantly enhanced organic C and N contents in SOM, free LF, iPOM, mSOM compared with bare flat and increased the proportion of allocated C in iPOM compared with S. salsa and P. australis soils (0–0.30 m depth). The proportion of the S. alterniflora-derived C in free LF and iPOM were significantly higher than that in mSOM, and the highest S. alterniflora-derived C content was found in iPOM of S. alterniflora soil. The most enriched ␦15 N values were found in S. alterniflora soil. Increased ␦15 N values and decreased C:N ratios from the free LF to iPOM to mSOM in S. alterniflora soil indicated a greater degree of decomposition. The results suggest that 10-year S. alterniflora invasion significantly alters soil organic C and N pools sizes and stability through changing plant residuals input, physical distribution of S. alterniflora-derived C and C turnover in SOM fractions. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Soil organic matter (SOM) contains huge carbon (C) and nitrogen (N) pools in terrestrial ecosystems (Sollins et al., 2009), and plays a critical role in global C (Amundson, 2001; Throop et al., 2013) and N cycling (Sollins et al., 2009). Any alteration to the SOM pool may evoke changes in greenhouse gas levels and potentially impacts the climate (Cheng et al., 2011; Throop et al., 2013). However, plant invasion, a growing threat to native ecosystems (in terms of stability, biodiversity, processes and functions) in many parts of the world (Ehrenfeld, 2003; Fernandes et al., 2014), could affect net primary production, nutrient input to the soil (e.g., litter of invasive

∗ Corresponding author at: School of Life Science and Institute of Wetland Ecology, Nanjing University, No. 22 Hankou Rd., Nanjing 210093, Jiangsu, PR China. Tel.: +86 25 83594560; fax: +86 25 83594560. ∗∗ Corresponding author. Tel.: +86 27 87510881; fax: +86 27 87510251. E-mail addresses: [email protected] (S. An), [email protected] (X. Cheng). http://dx.doi.org/10.1016/j.ecoleng.2015.11.010 0925-8574/© 2015 Elsevier B.V. All rights reserved.

plant and epiphyte, exudates) and litter decomposition in native ecosystems (Liao et al., 2007). This could ultimately influence SOM formation and turnover (Liao et al., 2006). The effects of plant invasion on C and N pools in SOM are drawing increased attention (Jackson et al., 2002; Hughes et al., 2006; Liao et al., 2006; Strickland et al., 2010). Previous studies have reported that plant invasion can enhance soil C and N sequestration due to increased above- and below-ground biomass inputs into the soil and/or decreased litter decomposition (Hibbard et al., 2001; Liao et al., 2006; Zhang et al., 2010). Conversely, some studies have shown that plant invasion causes soil C and N loss (Johnson and Wedin, 1997; Jackson et al., 2002; Strickland et al., 2010) or no significant change (McCarron et al., 2003; Hughes et al., 2006). These inconsistent results may be that the response of C and N pools in SOM to plant invasion may be influenced by multiple factors, including the quality and quantity of the litter and roots, litter decomposition rate (Liao et al., 2007), as well as soil C and N mineralization (Yang et al., 2013). Therefore, understanding how plant invasion both impact C and N pools sizes in SOM and control the

W. Yang et al. / Ecological Engineering 86 (2016) 174–182

stability and turnover of C and N pools in SOM is important for predicting long-term ecosystem C and N cycling. However, accurately detecting the influence of plant invasion on C and N pools sizes, stability and turnover in SOM of native ecosystems is difficult as SOM is a complex entity with distinct fractions characterized by different turnover times and degrees of physical and chemical stability (Del Galdo et al., 2003; Cheng et al., 2011; Herold et al., 2014). Combining physical SOM fractionation techniques with stable isotope analyses provides an effective approach for examining changes in C content and sources of input for SOM fractions and assessing C stability following plant invasion (Throop et al., 2013). Physical fractionation techniques can be used to separate bulk soil into free light fraction (LF), intra-aggregate particulate organic matter (iPOM) and mineral-associated organic matter (mSOM) (Six et al., 1998). According to the evidence that Wander (2004) and Marín-Spiotta et al. (2008) have reported that free LF and iPOM were considered to represent the soil active and the slowly mineralized pools, respectively. mSOM is considered to be representative of soil passive pool and ultimately determines long-term soil C and N sequestration due to its interactions with mineral surfaces (Kögel-Knabner et al., 2008; Schulze et al., 2009). ␦13 C values between C4 plants (mean ␦13 C ≈ −11‰) and C3 plants (mean ␦13 C ≈ −27‰) produce distinct isotopic signatures in SOM and its fractions (Cheng et al., 2011). Based on the alterations in the ␦13 C values of SOM and its fractions following changes to the vegetation, C4 -derived C contribution ratio and turnover rate of C in SOM and its fractions were quantified according to an isotope mass balance equation (Del Galdo et al., 2003; Liao et al., 2006; Cheng et al., 2011). In addition, soil ␦15 N was demonstrated to be able to be used as a tracer for N cycling processes and is a potential indicator of SOM quality (Robinson, 2001; Bijoor et al., 2008; Dou et al., 2013). For example, increased soil ␦15 N values revealed enhanced rates of N cycling accompanied by N losses (Billings, 2006; Dou et al., 2013). Soil ␦15 N values become enriched with higher degrees of SOM decomposition and humification (Templer et al., 2007; Marin-Spiotta et al., 2009). Spartina alterniflora, a perennial C4 grass native to North America, was introduced to China for beach protection purposes in 1979 (Xu and Zhuo, 1985). S. alterniflora reproduction contains sexual propagation by seed and clonal propagation by rhizome and vegetative fragmentation (Daehler and Strong, 1994), which plays an important role in exploiting new habitats (Wang et al., 2006). Due to its rapid growth, S. alterniflora has dispersed broadly from Tianjin in the north to Beihai in the south and covers a total area of approximately 112,000 ha (An et al., 2007). Suaeda salsa and Phragmites australis are annual and perennial C3 grass, respectively. Currently, S. alterniflora has rapidly expanded by occupying bare flat and replacing S. salsa and P. australis to become one of dominant plants in east coast of China (An et al., 2007). Previous studies have found S. alterniflora has higher leaf area index and net photosynthetic rate, and greater net primary production (Liao et al., 2007), well-developed root system compared to native species (Wang et al., 2006), and hence impacts ecosystem C and N stocks (Liao et al., 2007; Cheng et al., 2008), alters ecosystem–atmosphere exchange of CH4 , CO2 and N2 O (Yuan et al., 2015), as well as soil physicochemical properties (Yang et al., 2013) in coastal wetlands of China. However, little is known about the impacts of S. alterniflora invasion on soil organic C and N pools sizes, stability and turnover in SOM and its fractions. We hypothesized that S. alterniflora invasion could significantly affect soil organic C and N pools sizes and stability through changing plant residuals input, physical distribution of S. alterniflora-derived C and C turnover in SOM fractions. To test this hypothesis, soil C and N contents, ␦13 C and ␦15 N values of SOM and its fractions were examined in 10 years S. alterniflora community compared to bare flat, S. salsa and P. australis communities in a coastal salt marsh of eastern

175

China. The objectives of this study were to: (1) quantify soil organic C and N pools sizes and the contribution of S. alterniflora-derived C inputs to SOC in SOM and its fractions following S. alterniflora invasion; and (2) estimate soil organic C and N pools stability and C turnover following S. alterniflora invasion. 2. Materials and methods 2.1. Site descriptions The study was conducted in the core region of the Jiangsu Yancheng Wetland National Nature Reserve, Rare Birds (JYWNNRRB) (32◦ 48 47 –34◦ 29 28 N, and 119◦ 53 45 –121◦ 18 12 E) (Fig. 1). The total area of JYWNNRRB is about 247,260 ha, the core area of JYWNNRRB is about 22,596 ha, the buffer area of JYWNNRRB is about 56,742 ha, and the experimental area of JYWNNRRB is about 167,922 ha. JYWNNRRB is the first and largest coastal wetland conservation zone in China (Wang and Wall, 2010; Yang et al., 2013). JYWNNRRB is made up of aggrading mudflats with a mean annual temperature of approximately 13.8 ◦ C, mean annual precipitation of approximately 1000 mm (Mao et al., 2010), and mean annual seawater salinity of approximately 3.09% (Zhou et al., 2009). JYWNNRRB was designated as an internationally important wetland site (Ramsar) in 2002, and it plays a key role in protecting waterfowl (e.g., Grus japonensis) and other fauna, as well as natural mudflat wetlands (Wang and Wall, 2010). S. alterniflora was transplanted to the bare flat of the JYWNNRRB in 1983, and it rapidly expanded to form large areas of S. alterniflora salt marshes over the next 30 years (Zhang et al., 2004). The seaward S. alterniflora region is bare flat, that is there was no vegetation before the S. alterniflora invasion (Yang et al., 2013). Bare

Fig. 1. Location of the sampling site in Jiangsu Yancheng Wetland National Nature Reserve, Rare Birds (JYWNNRRB), China. Vegetation type succession in JYWNNRRB from sea to inland including bare flat, S. alterniflora, S. salsa and P. australis communities.

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Fig. 2. Flow chart of soil size and density fractionation adopted in this study, modified after John et al. (2005).

flat, S. alterniflora and S. salsa communities are in the lower, middle and high regions of the intertidal zone, respectively, and P. australis community is in the supralittoral zone (Yuan et al., 2015). Accordingly, JYWNNRRB has a clear distribution of vegetation succession from the sea to inland, i.e., from bare flat to S. alterniflora community to S. salsa community to P. australis community (Fig. 1; Yang et al., 2013). There is little overlap between the distributions of the vegetation communities (Zhou et al., 2009).

(Yang et al., 2013). The bulk density was measured using cutting ring method. Soil pH was determined at a 1:2 (soil:water) suspension (Fu et al., 2015). Soil EC was determined at a 1:5 (soil:water) mixture with a conductivity meter (Yang et al., 2013).

2.2. Soil and plant sampling

Soil free LF, iPOM and mSOM were obtained according to soil size and density fractionation procedure which referenced from Gregorich and Ellert (1993), Six et al. (1998) and Wu et al. (2004), and summarized in Fig. 2. A 25 g soil subsample was weighed and suspended in 50 mL of 1.70 g mL−1 NaI in a 100 mL centrifuge tube. The centrifuge tube was stoppered and shaken at 200 rpm for 1 h, and the materials that adhered to the stopper and sides of the centrifuge tube were washed into suspension with 3–5 mL NaI. The suspended sample was centrifuged at 1000 g for 20 min. The floating materials (free LF) were aspirated onto a 0.45 ␮m nylon filter with a vacuum pump, rinsed with 75 mL of 0.01 M CaCl2 followed by at least 75 mL of ultrapure water, and dried at 50 ◦ C. The floating materials in the centrifuge tube were extracted twice with NaI, and the two sub-fractions were mixed thoroughly to form a free LF sample and weighed (Gregorich and Ellert, 1993; Wu et al., 2004). The precipitation in the centrifuge tube was heavy fraction (HF), which was washed twice with 50 mL ultrapure water and dispersed in 0.5% sodium hexametaphosphate (SHMP) by shaking for 18 h on a reciprocal shaker. The dispersed heavy fraction was passed through a 53-␮m sieve. The materials remaining on the sieve, the intraaggregate particulate organic matter (iPOM) + sand, were dried at 50 ◦ C and weighed (Six et al., 1998). The soil and water mixture that passed through a 53-␮m sieve was poured into the centrifuge tube. The mineral-associated organic matter (mSOM) + clay + silt was obtained through centrifugation and decantation of the supernatant using ultrapure water to remove SHMP, dried at 50 ◦ C and weighed.

Three parallel transects, 5 km long and 50 m wide, along a vegetation succession gradient from bare flat (i.e., the control, no input of organic matter from vegetation) to S. alterniflora community to S. salsa community to P. australis community in JYWNNRRB were selected in November, 2012 (Fig. 1). The sampled transects which were covered by S. alterniflora community were bare flat before 2002 (Yao et al., 2010). Within each transect, four locations were marked from bare flat to S. alterniflora, S. salsa and P. australis communities (Fig. 1). Five 2 m × 2 m plots were randomly selected in each location, and three soil cores (0.05 m diameter × 0.30 m depth) were randomly collected in each plot. The soil cores from each plot were thoroughly mixed to form a composite sample. Three 0.50 m × 0.50 m quadrats were randomly established to collect plant leaves and litter, and three soil sampling blocks (0.15 m length × 0.15 m width × 0.30 m depth) were excavated to obtain the root biomass in S. alterniflora, S. salsa and P. australis communities in each location, respectively. Each soil sampling block was put through a 100 mesh sieve and rinsed thoroughly with water, and the roots that remained in the sieve were collected. The collected leaves, litter and roots were cleaned and dried at 65 ◦ C to a constant weight. Plant residuals were removed from the soil samples, and the soil samples were passed through a 2 mm sieve and oven-dried at 50 ◦ C. Fresh soil subsample was oven dried at 105 ◦ C to determine soil moisture

2.3. Soil size and density fractionation

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Table 1 Soil (0–0.30 m depth) physicochemical properties (mean ± SE, n = 15) in bare flat, S. alterniflora, S. salsa and P. australis communities in a coastal salt marsh of eastern China. Statistically significant differences from one-way ANOVA are shown. Different letters indicate statistically significant differences at the ˛ = 0.05 level among the communities. Community

Moisture (%)

Bulk density (g cm−3 )

pH

EC (s/m)

Bare flat S. alterniflora S. salsa P. australis Source of variation Community

25.80 ± 0.35 45.90 ± 2.21a 29.48 ± 0.81b 26.28 ± 0.31b

1.57 ± 0.01a 1.25 ± 0.03b 1.55 ± 0.01a 1.64 ± 0.01a

8.87 ± 0.02b 8.59 ± 0.03c 9.14 ± 0.03a 9.17 ± 0.04a

0.225 ± 0.012b 0.633 ± 0.057a 0.229 ± 0.008b 0.166 ± 0.009b

***

***

***

***

b

Note: *** P < 0.001. EC: Electrical conductivity.

2.4. Carbon and nitrogen concentrations and isotope analyses Samples of leaves, litter, roots, whole soil, free LF, iPOM and mSOM fractions obtained from Section 2.3. soil size and density fractionation procedures were dried to a constant weight and passed through 100-mesh sieves. Subsamples of whole soil and its fractions were treated with 1 N HCl at room temperature for 24 h to eliminate total inorganic carbon. The ␦13 C and ␦15 N values, C and N concentrations for subsamples of the leaves, litter, roots, whole soil and its fractions were determined using an IsoPrime100 isotope ratio mass spectrometer (Isoprime Ltd., Cheadle Hulme, UK) coupled to a vario PYRO cube elemental analyzer (Elementar Analysensystem GmbH, Hanau, Germany). C and N isotope ratios were indicated by ı X as follows: ıX =

 R  SAMPLE RSTANDARD



–1 × 1000 ‰

(1)

where X stands for either C or N, RSAMPLE = (13 C/12 C) or (15 N/14 N) ratio of the sample, and RSTANDARD = 13 C/12 C ratio of the Pee Dee Belemnite (PDB) standard, or 15 N/14 N ratio of atmospheric N2 . The accuracy of repeat measurements was ± 0.13‰ for ␦13 C and ± 0.21‰ for ␦15 N. The proportion of S. alterniflora-derived C (fnew ) in SOM, free LF, iPOM and mSOM was determined using the mass balance equation (Del Galdo et al., 2003; Dou et al., 2013)



fnew =

ınew –ıold ımix –ıold



× 100%

(2)

where ınew is the ␦13 C value of SOM, free LF, iPOM and mSOM in S. alterniflora soil, ıold is the ␦13 C value of SOM, free LF, iPOM and mSOM in bare flat, assuming that the C input ratio has remained relatively stable in bare flat in the past 10 years, and ımix is the ␦13 C value of the mixed S. alterniflora residue, and is a weighted average based on the different masses of the different plant material types (leaves, litter, and roots). The S. alterniflora-derived C content (Ccontent SA-derived , g m−2 ) of SOM, free LF, iPOM and mSOM in S. alterniflora soil was calculated as follows: Ccontent SA-derived = Ccontent × fnew

(3)

where Ccontent is the C content of SOM, free LF, iPOM and mSOM in S. alterniflora soil, and fnew is the proportion of S. alterniflora-derived C in SOM, free LF, iPOM and mSOM. Decomposition rate (k) of old C (i.e., soil organic C (SOC) before S. alterniflora invasion) (year−1 ) in SOM, free LF, iPOM and mSOM of S. alterniflora soil were calculated using a first-order decay model (Six et al., 1998; Six and Jastrow, 2002; Cheng et al., 2007): At = A0 e−kt

(4)

and k=−

ln(At /A0 ) t

(5)

where At is the original SOC remaining after t years [At = (1 − fnew ) Ccontent at time t], A0 is the SOC content before S. alterniflora invasion [A0 = SOC content of bare flat], t is the time since S. alterniflora invasion, 10 years used in this study, and assuming that decomposition rate (k) of old C follows first-order kinetics at steady-state conditions (Cheng et al., 2007).

2.5. Statistics Data were tested for normality and log- or cube roottransformed to satisfy the assumptions for statistical analysis. One-way ANOVA was used to analyze significant differences between communities for C and N contents, ␦13 C and ␦15 N values, C:N ratios in SOM, free LF, iPOM and mSOM, soil mass percent of SOM fractions, proportions of C and N allocated to SOM fractions, ␦13 C and ␦15 N levels, C:N ratios, biomass in plant materials, and each soil physicochemical property. Significant differences in soil mass percent and C:N ratios among soil fractions in each community and the proportion of S. alterniflora-derived C, S. alterniflora-derived C content and decay rate (k) of old C among soil fractions in S. alterniflora soil were examined by one-way ANOVA. The differences in the group means were examined using Duncan significant difference test with a significance level of P < 0.05. Linear regression analysis was conducted to correlate C and N contents of all soil fractions with litter and root biomass. All data analyses were performed using SPSS 19.0.

3. Results 3.1. Soil physicochemical properties and plant biological traits Soil moisture and EC in S. alterniflora soil were significantly higher than those in bare flat, S. salsa and P. australis soils, but the pH and bulk density in S. alterniflora soil were significantly lower than that in bare flat, S. salsa and P. australis soils (Table 1). Root (0–0.30 m depth) and litter biomass in the S. alterniflora community were significantly higher than those in S. salsa and P. australis communities (Table 2). However, there were no significant differences in root and litter biomass between S. salsa and P. australis communities (Table 2). The ␦13 C values of leaves, litter and roots in S. alterniflora community varied from −13.60‰ to −13.74‰, which was typical of C4 plants whereas the ␦13 C values of C3 plants, S. salsa and P. australis, varied from −27.05‰ to −29.45‰ (Table 2). The ␦15 N values of S. alterniflora, S. salsa and P. australis plant materials varied from 2.70‰ to 4.27‰, 0.33‰ to 2.35‰ and −0.70‰ to 1.17‰, respectively (Table 2). The leaves and litter C:N ratios in S. alterniflora were significantly higher than those in S. salsa, and the C:N ratio of the roots in S. alterniflora was higher than that in P. australis (Table 2).

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Table 2 The ␦13 C and ␦15 N values, C:N ratio and the biomass (mean ± SE, n = 9) of S. alterniflora, S. salsa and P. australis plants in a coastal salt marsh of eastern China. Statistically significant differences from one-way ANOVA are shown. Different letters indicate statistically significant differences at the ˛ = 0.05 level among the three species. Variable

Plant part

␦ C (‰)

Species

Leaves Litter Roots Leaves Litter Roots Leaves Litter Roots Leaves Litter Roots

13

␦15 N (‰)

C:N ratio

Biomass (g m−2 )

S. alterniflora (C4 plant)

S. salsa (C3 plant)

P. australis (C3 plant)

−13.74 −13.60 −13.70 4.27 2.91 2.70 47.60 54.62 46.93 426 353 5808

−28.63 −28.27 −29.45 2.35 0.33 1.41 21.47 27.77 44.85 106 31 1128

−27.60 −27.63 −27.05 1.17 −0.70 0.38 47.62 55.88 34.63 97 76 1763

± ± ± ± ± ± ± ± ± ± ± ±

a

0.05 0.05a 0.14a 0.20a 0.45a 0.11a 3.63a 2.40a 1.11a 71a 62a 601a

± ± ± ± ± ± ± ± ± ± ± ±

b

0.14 0.06b 0.21c 0.43b 0.46b 0.44b 2.20b 1.50b 4.90ab 16b 3b 149b

± ± ± ± ± ± ± ± ± ± ± ±

0.52b 0.33b 0.23b 0.23c 0.18b 0.19c 2.97a 4.32a 1.86b 10b 12b 315b

Table 3 The ␦13 C (‰) and ␦15 N (‰) values (mean ± SE, n = 15) of soil fractions in bare flat, 10-year invaded S. alterniflora, S. salsa and P. australis soils (0–0.30 m depth) in a coastal salt marsh of eastern China. Statistically significant differences from one-way ANOVA are shown. Different letters indicate statistically significant differences at the ˛ = 0.05 level among the communities. Community

␦13 C (‰)

␦15 N (‰)

SOM

free LF

iPOM

mSOM

SOM

free LF

iPOM

mSOM

Bare flat S. alterniflora S. salsa P. australis Source of variation Community

−21.11 ± 0.78b −18.41 ± 0.35a −24.10 ± 0.35c −24.97 ± 0.07c

−24.13 ± 0.03b −17.39 ± 0.28a −26.91 ± 0.19c −26.61 ± 0.17c

−23.23 ± 0.02b −17.45 ± 0.45a −26.41 ± 0.21c −26.22 ± 0.09c

−23.77 ± 0.10b −20.96 ± 0.17a −24.02 ± 0.13b −24.88 ± 0.07c

0.48 ± 0.49c 3.93 ± 0.29a 3.13 ± 0.06ab 2.37 ± 0.10b

1.11 ± 0.16c 3.68 ± 0.28a 2.37 ± 0.28b 2.06 ± 0.13b

−0.08 ± 0.87c 3.79 ± 0.38a 2.10 ± 0.25ab 1.32 ± 0.12bc

−0.04 ± 0.67c 4.18 ± 0.24a 3.60 ± 0.21ab 2.86 ± 0.07b

*

***

*

***

***

***

**

*

SOM: Soil organic matter; free LF: free light fraction; iPOM: intra-aggregate particle organic matter; mSOM: mineral-associated SOM. Note: * P < 0.05; ** P < 0.01; *** P < 0.001.

3.2. The ı13 C and ı15 N values of SOM, free LF, iPOM and mSOM free LF-C / SOC (%)

(d)

P > 0.05

80

80

60

60

40 20

40 a b

ab

a

P < 0.001

(e)

ab

a

a

a

iPOM-C / SOC (%)

0

0 (b)

80 60

a

80 60

a b

b

b

b

b

20

40 20

0 mSOM-C / SOC (%)

P < 0.05

a

40

P < 0.05 ab a

(c) 80 60

20

c

bc

0 (f) a

a

P < 0.05 a

b

80 60

40

40

20

20

0

mSOM-N / SON (%)

C and N contents of mSOM accounted for the largest fraction (52.6–71.6%) of total SOM across communities, except for the N content of mSOM in bare flat, whereas C and N contents of free LF accounted for the smallest fraction of total SOM across communities (Fig. 3). C and N contents of SOM, iPOM and mSOM in S. alterniflora soil were considerably higher than those in other soils, and C and N contents of free LF in S. alterniflora soil were higher compared with bare flat (Table 4). The free LF-C/SOC in S. alterniflora soil was significantly lower than that in bare flat (Fig. 3a). The iPOM-C accounted for 40.9% of the total SOC content in S. alterniflora soil, which was significantly higher than that in S. salsa and P. australis soils (Fig. 3b) even though S. alterniflora soil had the lowest mass proportion of iPOM among communities (Fig. 4). Although S. alterniflora soil had the highest mass proportion of mSOM among communities (Fig. 4), the mSOM-C accounted for 56.8% of the total SOC content in S. alterniflora soil, which was significantly lower than that in S. salsa soil (Fig. 3c). The C:N ratio of SOM, iPOM and mSOM significantly increased in S. alterniflora soil in comparison with other soils, and

P > 0.05

iPOM-N / SON (%)

3.3. C and N contents of SOM, free LF, iPOM and mSOM

100 (a)

free LF-N / SON (%)

The ␦13 C values of SOM, free LF, iPOM and mSOM in S. alterniflora soil were significantly higher than those in bare flat, S. salsa and P. australis soils (Table 3). The ␦15 N values of SOM, free LF, iPOM and mSOM in S. alterniflora soil were significantly higher compared with bare flat and P. australis soils (Table 3). There was no statistically significant difference in the ␦15 N values of organic soil between S. alterniflora and S. salsa soils except for free LF (Table 3).

100

0 BF

SA

SS

PA

BF

SA

SS

PA

Communities Fig. 3. The proportion of C and N contents allocated (mean ± SE, n = 15) in free LF, iPOM and mSOM of bare flat, 10-year invaded S. alterniflora, S. salsa and P. australis soils (0–0.30 m depth). Different letters over the bars indicate statistically significant differences at the ˛ = 0.05 level among communities. BF = bare flat; SA = Spartina alterniflora; SS = Suaeda salsa; PA = Phragmites australis. SOC = Soil organic carbon; SON = Soil organic nitrogen; SOM = Soil organic matter; free LF = free light fraction; iPOM = intra-aggregate particle organic matter; mSOM = mineral-associated SOM.

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Table 4 Soil organic C and N contents (mean ± SE, n = 15) of soil fractions in bare flat, 10-year invaded S. alterniflora, S. salsa and P. australis soils (0–0.30 m depth) in a coastal salt marsh of eastern China. Statistically significant differences from one-way ANOVA are shown (n.s. = not significant). Different letters indicate statistically significant differences at the ˛ = 0.05 level among the communities. C (g C m−2 )

Community

N (g N m−2 )

SOM

Free LF

iPOM

449 ± 9 3783 ± 218a 2044 ± 208b 1684 ± 108b

28 ± 7 71 ± 5a 83 ± 16a 74 ± 15a

177 ± 6 1547 ± 90a 503 ± 59b 441 ± 61b

236 ± 9 2153 ± 157a 1450 ± 122b 1158 ± 62b

102.9 ± 14.9 380.3 ± 44.8a 277.8 ± 6.5b 237.0 ± 11.5b

1.0 ± 0.2 4.0 ± 0.3a 5.6 ± 1.5a 4.7 ± 1.0a

51.8 ± 3.4 105.7 ± 4.6a 63.9 ± 16.7b 49.0 ± 9.8b

41.8 ± 3.5c 265.6 ± 28.4a 199.4 ± 15.4b 160.2 ± 4.8b

***

*

***

***

***

n.s.

n.s.

***

c

Bare flat S. alterniflora S. salsa P. australis Source of variation Community

b

mSOM c

SOM c

free LF c

iPOM b

mSOM b

See Table 3 for abbreviations. Note: * P < 0.05; *** P < 0.001. Table 5 Linear regression analysis of C and N contents in SOM, LF, iPOM and mSOM against litter and root biomass across the communities. Regression analysis with litter biomass

−2

SOM—C (g m ) free LF—C (g m−2 ) iPOM—C (g m−2 ) mSOM—C (g m−2 ) SOM—N (g m−2 ) free LF—N (g m−2 ) iPOM—N (g m−2 ) mSOM—N (g m−2 )

2

Regression analysis with root biomass

Equation

R

P

Equation

R2

P

Y = 5.761X + 1613.094 Y = −0.031X + 80.882 Y = 3.213X + 333.673 Y = 2.573X + 1189.421 Y = 0.405X + 235.773 Y = −0.004X + 5.369 Y = 0.146X + 50.265 Y = 0.284X + 164.471

0.854 0.062 0.901 0.761 0.754 0.140 0.593 0.726

<0.001 0.517 <0.001 0.002 0.002 0.322 0.015 0.004

Y = 0.407X + 1323.508 Y = −0.002X + 82.649 Y = 0.234X + 151.222 Y = 0.174X + 1081.320 Y = 0.025X + 226.982 Y = −0.0003X + 5.603 Y = 0.011X + 41.949 Y = 0.018X + 157.630

0.815 0.064 0.916 0.669 0.533 0.146 0.604 0.527

0.001 0.513 <0.001 0.007 0.025 0.310 0.014 0.027

See Table 3 for abbreviations.

the C:N ratios decreased from free LF to iPOM to SOM to mSOM in S. alterniflora soil (Fig. 5). The C and N contents of SOM, iPOM and mSOM were significantly correlated with litter and root biomass (Table 5). 3.4. Soil C turnover The proportion of S. alterniflora-derived C in free LF (64.55%) and iPOM (60.55%) was significantly higher than that in SOM (36.36%) and mSOM (27.96%) (Fig. 6a). However, the S. alterniflora-derived C content was greatest in iPOM followed by mSOM and free LF in S. alterniflora soil (Fig. 6b). The decomposition rate of old C was faster in free LF and iPOM than in mSOM of S. alterniflora soil (Fig. 6c).

100 80 A a

60

A a

B B b B b c

iPOM

10

mSOM

SOM fractions Fig. 4. Mass proportion (mean ± SE, n = 15) of free LF, iPOM and mSOM in bulk soil (0–0.30 m depth) of bare flat, 10-year invaded S. alterniflora, S. salsa and P. australis communities. Different lower case letters over the bars indicate statistically significant differences at the ˛ = 0.05 level among communities in each soil fraction. Different upper case letters over the bars indicate statistically significant differences at the ˛ = 0.05 level among SOM fractions in each community. See Fig. 1 for abbreviations.

AA b bA b

20

C C C C b a a a free LF

P < 0.05

30

40

0

40

AA a ab A b

BF SA SS PA B c

20

Whole soil organic C and N contents increased 0.37–7.43-fold after 10 years of S. alterniflora invasion in comparison to bare flat and native S. salsa and P. australis communities in a coastal salt marsh of eastern China (Table 4). Increased whole soil organic C and N contents in the S. alterniflora community were primarily due to increases in C and N in mSOM and iPOM fractions (Table 4). Soil C and N sequestration following plant invasion is largely determined by the amount of litter and root biomass input into the soil (Hibbard et al., 2001; Liao et al., 2006). This evidence was supported by that the S. alterniflora community had greater litter and root biomass compared with S. salsa and P. australis

C:N ratio

Percent of soil mass (%)

P < 0.05

4. Discussion

B a BB bb

C a BB b B b c

BF SA SS PA

B c

D BaB aB a b

0 SOM

free LF

iPOM

mSOM

Soil fractions Fig. 5. The C:N ratio (mean ± SE, n = 15) of SOM, free LF, iPOM and mSOM in bare flat, 10-year invaded S. alterniflora, S. salsa and P. australis soils (0–0.30 m depth) in a coastal salt marsh of eastern China. Different lower case letters over the bars indicate statistically significant differences at the ˛ = 0.05 level among communities in each soil fraction. Different upper case letters over the bars indicate statistically significant differences at the ˛ = 0.05 level among soil fractions in each community. See Fig. 1 for abbreviations.

W. Yang et al. / Ecological Engineering 86 (2016) 174–182

-1 Decomposition rate (k) of old C (year )

S. alterniflora-derived C content (g m-2)

Proportion of S. alterniflora-derived C (%)

180

100 (a)

P < 0.001

80 a

a

60 b

40

b 20 0 1600

(b)

a

P < 0.05

1400 1200

b

1000 800

c

600 400 200

d

0

a (c)

a

.10

P < 0.001

.08 .06

b

.04

b

.02 0.00 SOM

LF

iPOM

mSOM

Soil fractions Fig. 6. (a) Proportion of S. alterniflora-derived C, (b) S. alterniflora-derived C content and (c) Decomposition rate (k, year−1 ) of old C (mean ± SE, n = 15) of SOM, free LF, iPOM and mSOM in 10-year invaded S. alterniflora soil (0–0.30 m depth). Different letters over the bars indicate statistically significant differences at ˛ = 0.05 level among soil fractions.

communities (Table 2). Indeed, soil C and N contents in SOM, iPOM and mSOM were strongly related to litter and root biomass (Table 5), which demonstrated that substantial S. alterniflora debris entering the soil would accelerate C and N sequestration in SOM, iPOM and mSOM (Table 4). Additionally, the highest soil moisture was found in S. alterniflora soil (Table 1), which was more beneficial to SOM accumulation by provided anaerobic soil conditions for long-term storage of SOM in wetlands (Whitting and Chanton, 2001). S. alterniflora invasion also significantly increased C and N contents in free LF compared with bare flat (Table 4), whereas free LF-C/SOC in S. alterniflora soil was significantly lower than that in bare flat (Fig. 3a). These results are consistent with the previous finding that S. alterniflora invasion considerably raised the concentrations of the SOC labile pool fractions but decreased labile SOC/SOC relative to bare flat in a coastal wetland of eastern China (Yang et al., 2013). The low free LF-C/SOC ratio in S. alterniflora soil was primarily due to poorer-quality S. alterniflora residuals (i.e., higher C:N ratio of S. alterniflora materials) (Yang et al., 2015), and more recalcitrant to decomposition (e.g., high contents of K, Na, Ca, Mg and lignocellulosic material) (Yang et al., 2009). iPOM consists of partially decomposed organic materials and is protected within the soil aggregate structure (Leifeld and KögelKnabner, 2005). The mSOM is composed of highly humified organic

residues and is protected by organic-mineral interactions with silts and clays (Kögel-Knabner et al., 2008). Higher proportion of C allocated in iPOM and lower proportion of C allocated in mSOM were found in S. alterniflora soil compared to S. salsa and/or P. australis soils (Fig. 3b and c), leading to lower physical SOC stabilization in S. alterniflora soil. Previous studies have indicated that plant materials are first incorporated into the coarse soil fraction (e.g., macro-aggregates) and are then transferred from the coarse to the fine soil fraction (e.g., silts and clays) (Desjardins et al., 2006; Schwendenmann and Pendall, 2006), the fine soil fraction obtains a stable accumulation of SOM (Desjardins et al., 2006; Zhang et al., 2010). Hence, the increased proportion of C allocated in iPOM and the decreased proportion of C allocated in mSOM in S. alterniflora soil was expected as substantial S. alterniflora residues were more rapidly incorporated into iPOM than into mSOM. The S. alterniflora residues were also resistant to decomposition (Liao et al., 2007; Yang et al., 2009, 2015), indicating the soil microbes were not easier to translate it into mSOM compared to S. salsa and P. australis residues. Our stable isotopic analyses indicated that the ␦13 C values of all soil fractions in S. alterniflora soil were significantly higher than those in bare flat, S. salsa and P. australis soils (Table 3), partly owing to the contribution of S. alterniflora residuals (Fig. 6a). The proportion of S. alterniflora-derived C in free LF and iPOM was significantly higher than that in the mSOM of S. alterniflora soil (Fig. 6a). This may because free LF and iPOM are mostly composed of undecomposed and partially decomposed plant materials (Gregorich et al., 2006), and iPOM-C was more influenced by litter and roots input than mSOM (Table 5). Interestingly, S. alterniflora-derived C content was greatest in iPOM followed by the mSOM and free LF in S. alterniflora soil (Fig. 6b), which suggests that S. alterniflora-derived C would not easily convert from iPOM to mSOM in the short-term. This may be due to the inherently more resistant nature of the S. alterniflora residuals (Yang et al., 2009), and the more anaerobic salt marsh conditions (Table 1, Zhang et al., 2010). Even though mSOM had the lowest proportion of S. alterniflora-derived C, S. alterniflora-derived C content in mSOM was significantly higher than that in free LF of S. alterniflora soil (Fig. 6a and b), which is probably due to free LF is not protected by aggregates or soil minerals although it had the greatest C input rate (Fig. 6a), and is easily accessible to microbes that induce the rapid loss of SOM (Fig. 6c; John et al., 2005; Cheng et al., 2011), while mSOM is the most stable SOM fraction compared to free LF and iPOM through its interaction with mineral surfaces (e.g., iron/aluminum oxides and hydroxides) (Kögel-Knabner et al., 2008; Schulze et al., 2009), it is resistant to decomposition (Fig. 6c; Liao et al., 2006). Thus, a lower decomposition rate of old C in mSOM may compensate some decrease in S. alterniflora-derived C input and ultimately promote S. alterniflora-derived C sequestration in mSOM relative to free LF. The ␦15 N values of all soil fractions in S. alterniflora soil were greater than those in bare flat and P. australis soils (Table 3). One possible explanation was that the mean ␦15 N values of S. alterniflora plant materials were significantly higher than those in S. salsa and P. australis plant materials (Table 2), and hence, a large quantity of S. alterniflora residuals entering the soil would enrich the ␦15 N value of S. alterniflora soil. Another possible explanation was that the substantial S. alterniflora residuals input to the soil might increase the N turnover rate that causes labile N loss through N mineralization (Schade et al., 2001). The fast N loss rate and the high N level in S. alterniflora soil would explain the increase of ␦15 N. Additionally, the ␦15 N values increased from free LF to iPOM to mSOM in S. alterniflora soil (Table 3), reflecting an increasing degree of SOM decomposition (Liao et al., 2006; Cheng et al., 2011). The ␦15 N values increases because the decay of most organic materials (besides wood) follows a rise in aliphaticity, and a rise in aliphaticity follows ␦15 N enrichment (Kramer et al., 2003; Wagai et al., 2009). This

W. Yang et al. / Ecological Engineering 86 (2016) 174–182

result was supported by our finding that the C:N ratios declined from free LF to iPOM to mSOM in S. alterniflora soil (Fig. 5), which is consistent with previous studies that found that a declining C:N ratio in SOM fractions is closely related to increasing SOM decomposition and humification (John et al., 2005; Marin-Spiotta et al., 2009; Wagai et al., 2009). Finally, it is generally acknowledged that the C and N pools in SOM in a coastal salt marsh of eastern China (i.e., JYWNNRRB) were regulated not only by S. alterniflora invasion, but also by semidiurnal tidal (Zhou et al., 2009). Dissolved organic C and N of tidal water probably input to the salt marshes and influenced organic C and N content in S. alterniflora soil (Cheng et al., 2008). Gebrehiwet et al. (2008) have reported that the increased soil organic C and N in S. alterniflora salt marsh was partly owing to the contribution of phytoplankton. The increased C and N in SOM of S. alterniflora soil may result from a joint contribution of terrestrial and marine organic matters. A further study is necessary to precisely quantify the potential contribution of other sources except for S. alterniflora to SOM. Nevertheless, this study demonstrate that 10-year S. alterniflora invasion significantly impacts on SOM dynamics by altering soil organic C and N sequestration, stabilization and turnover. 5. Conclusions In summary, 10-year S. alterniflora invasion significantly enhanced whole soil organic C and N contents in comparison to bare flat, S. salsa and P. australis communities by primarily accumulating organic C and N contents in mSOM and iPOM of S. alterniflora soil. Higher proportion of C allocated in iPOM and lower proportion of C allocated in mSOM were found in S. alterniflora soil compared to S. salsa and/or P. australis soils, leading to lower physical SOC stabilization in S. alterniflora soil. The proportion of S. alternifloraderived C in free LF and iPOM was significantly higher than that in mSOM of S. alterniflora soil. The highest S. alterniflora-derived C content was found in iPOM of S. alterniflora soil. The most enriched ␦15 N values were found in S. alterniflora soil, which probably due to the high S. alterniflora residuals input and the fast N loss rate in S. alterniflora soil. Increased ␦15 N values and decreased C:N ratios from free LF to iPOM to mSOM in S. alterniflora soil imply a rising degree of humification. Our results suggested that short-term S. alterniflora invasion could alter soil C and N physical distribution and C turnover in SOM and its fractions, and ultimately affect soil organic C and N pools sizes and stability in a coastal salt marsh of eastern China. This highlighted the evidence that plant invasion can potentially affect ecosystem processes and functions (Mack et al., 2000; Ehrenfeld, 2003), especially the sequestration of soil organic C and N pools. Acknowledgements This research was financially supported by the National Basic Research Program of China (grant no. 2013CB430400). We thank Zhihui Shi for assistance with the fieldwork, Ying Wei for assistance with the laboratory analyses, and all of the members of the Jiangsu Yancheng Wetland National Nature Reserve for Rare Birds for supporting this research. Last but not least, we appreciate two anonymous reviewers and chief editor for their insightful comments and valuable suggestions on this paper. References Amundson, R., 2001. The carbon budget in soils. Annu. Rev. Earth Planet. Sci. 29, 535–562. An, S.Q., Gu, B.H., Zhou, C.F., Wang, Z.S., Deng, Z.F., Zhi, Y.B., Li, H.L., Chen, L., Yu, D.H., Liu, Y.H., 2007. Spartina invasion in China: implications for invasive species management and future research. Weed Res. 47, 183–191.

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