journa l h om epage: www.elsev ier .com/ locate /eco leng
hort communication
O2 evolution from standing litter of the emergent macrophyteeyeuxia angustifolia in the Sanjiang Plain, Northeast China
inhou Zhanga,b, Rong Maoa, Chao Gonga, Tianhua Qiaoa, Changchun Songa,∗
Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, ChinaUniversity of Chinese Academy of Sciences, Beijing 100049, China
r t i c l e i n f o
rticle history:eceived 25 June 2013eceived in revised form 20 October 2013ccepted 4 December 2013vailable online 29 December 2013
Microbial decay of emergent macrophyte litters in the standing-dead phase is an essential componentof litter decomposition and thus carbon (C) cycle in wetland ecosystems. In this study, we examined theamount of microbial respiration from standing litter in a Deyeuxia angustifolia-dominated marsh in theSanjiang Plain by integrating field studies with laboratory experiments. In the field, CO2 evolution fromstanding litter exhibited a pronounced diel pattern, with high evolution rates concurring with increasinglitter water potential at night. Notably, significant CO2 evolution even existed at temperature of −4 ◦C.Overall, rates of CO2 evolution showed strong positive correlations with relative humidity and litterwater potential. In the laboratory, rates of CO2 evolution from wetted culms and leaves increased withincreasing temperature, and the relationship between CO2 evolution rates and temperature could bewell described with an exponential model. Based on extrapolation from temperature-adjusted meanCO2 evolution rates and standing litter mass, annual CO2 fluxes of culms (3.07 g C m−2 yr−1) and leaves
−2 −1 −2 −1 −2 −1
(6.81 g C m yr ) accounted for 2.32% (culms, 132.30 g C m yr ) and 6.94% (leaves, 98.20 g C m yr )of the corresponding annual net aboveground production, respectively. In total, microbial mineralizationof standing litter only contributed to 1.12% of the ecosystem respiration (880 g C m−2 yr−1). Our resultshighlight the importance of standing-dead phase in litter decomposition and C cycle in wetlands, andalso suggest that CO2 flux from standing litter could even be neglected in assessing C budget in the D.angustifolia-dominated freshwater marshes in the Sanjiang Plain, Northeast China.
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. Introduction
In wetland ecosystems, many emergent macrophytes do notmmediately collapse into water or on the sediment surface follow-ng senescence, but remain in an aerial standing-dead position (theo-called ‘standing litter’) for a substantial period (Newell, 2001;uehn et al., 2004; Liao et al., 2008). Moreover, fungal decomposersenerally colonize the standing litter at the onset of plant senes-ence (Kuehn and Suberkropp, 1998a; Kuehn et al., 1999, 2011;ewell, 2001; Chimney and Pietro, 2006). Mineralization of stand-
ng litter may represent a short-circuit in wetland carbon (C) cycle,.e., the C fixed in plant biomass is lost directly to atmosphere with-
ut cycling through soil organic matter pools. Previous studies haveerified that CO2 flux from standing litter is an essential process ofetland C cycle, and thus is recognized as an important pathway of
∗ Corresponding author at: Northeast Institute of Geography and Agroecology,hinese Academy of Sciences, 4888 Shengbei Road, Changchun 130102, China.el.: +86 431 85542204; fax: +86 431 85542298.
reenhouse gas emissions in subtropical (e.g., Newell et al., 1996;uehn and Suberkropp, 1998b; Liao et al., 2008) and temperate
e.g., Welsch and Yavitt, 2003; Kuehn et al., 2004) wetlands. How-ver, little is known about the contribution of microbial respirationrom standing litter to litter decomposition and ecosystem CO2 fluxn wetlands.
The Sanjiang Plain, a floodplain in Northeastern China, inhabitsne of the largest freshwater marshes in China (Zhao, 1999; Wangt al., 2010). In this region, most marshes are dominated by emer-ent macrophytes, such as Deyeuxia angustifolia, Carex lasiocarpand Carex meyeriana. Previous studies have examined the decay ofhese macrophytes litters by placing plant matters into water or onediments surface in the freshwater marshes (e.g., Wu et al., 2007;
ang et al., 2009; Song et al., 2011). Still now, there is no infor-ation about the decomposition of litters in the standing-dead
hase in this area. Moreover, annual estimates of greenhouse gasesmission from marshes did not consider the contribution of stand-
ng litter-associated microbial respiration to ecosystem respiratione.g., Song et al., 2009; Zhang et al., 2005). In this study, taking a D.ngustifolia-dominated marsh as a model ecosystem, we examinedhe importance of microbially mediated mineralization of standing
itter in ecosystem respiration and C budget in freshwater marshesocated in the Sanjiang Plain, Northeast China.
. Materials and methods
.1. Study site
This study was conducted in a D. angustifolia-dominated fresh-ater marsh in the Sanjiang Plain, Northeast China (47◦35′ N,
33◦31′ E, 56 m a.s.l.). D. angustifolia is a perennial clonal grassith overwintering belowground rhizomes, generally formingure stands in seasonally inundated marsh and wet meadow.he climate belongs to the temperate continental monsoon of aeasonal frozen zone. Its mean annual temperature is 2.5 ◦C, pre-ipitation is approximately 558 mm, and frost-free period is 125ays. Mean above- and below-ground net plant production of thisarsh is approximately 480 and 300 g dry mass m−2 yr−1, respec-
ively. More detailed information on this study site is provided inong et al. (2009).
.2. Field experiments
Standing litter mass of D. angustifolia was measured monthlyrom September 2011 to August 2012. We established 5 permanentlots (4 m × 4 m) in this marsh, and then determined standing-deadhoot densities in the randomly selected quadrat (0.5 m × 0.5 m) inach plot. At each sampling date, 20 individual shoots were ran-omly collected in each plot and separated into leaves (including
eaf sheath) and culms. All shoot fractions were oven-dried at 65 ◦Cnd weighed. Standing litter mass was assessed by multiplyinghoot density with individual mass. The detailed standing litterass of leaves and culms were present in Appendix Fig. 1.Diel patterns of microbial CO2 evolution from standing litter
ere determined once a month in October 2011, April 2012 anduly 2012. We randomly chose 10 standing-dead shoots every 2 h inach permanent plot, and divided the shoots into leaves and culms.hen leaves and culms were respectively cut into 8 cm pieces,ixed carefully, and then divided into two subsamples. For both
eaves and culms, one subsample was further cut into 2 cm pieceso determine litter water potential using a dew-point microvolt-
eter (model HR-33T, Wescor), and another subsample was placedn glass incubation jars (250-mL) and sealed. Meanwhile, another 5ars without plant materials were sealed as controls. All sealed jars
ere placed in shade for 1 h to prevent direct sunlight from warm-ng jars. In the 1 h period, four gas samples (5 mL for each sample)
ere taken from the jars in 20-min intervals and analyzed for CO2oncentration on a gas chromatograph (HP 4890, Hewlett Packard,A, USA). Afterwards, all litter samples were oven-dried at 65 ◦Cnd weighed. Air temperature, relative humidity and precipitationere obtained by the adjacent automatic weather station.
.3. Laboratory experiments
CO2 evolution rates from wetted plant litter were determinedt a series of temperatures in October 2011, April 2012 and July012, respectively. Fresh litter samples (leaves, 2 g; culms; 3 g)ere placed into sterile Petri dishes (150 mm × 20 mm) containing
sterile filter paper, and each litter type was replicated 5 times.dditional 5 Petri dishes containing a filter paper without plantaterials were considered as controls. All Petri dishes were wet-
ed until saturation with sterile deionized water, placed into an
ncubator, pre-incubated for 2 h before litter samples and filterapers being placed into 250-mL glass incubation jars, sealed and
ncubated for 1 h at −5 ◦C. Then litter samples together with filterapers were taken back to Petri dishes. The incubator temperature
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as then increased in increments of 10 ◦C up to 35 ◦C allowing theame litter samples incubated at each temperature setting as pre-ious described. In each 1 h incubation period, gas samples wereaken and analyzed for CO2 concentration on a gas chromatograph.
.4. CO2 flux estimate
CO2 evolution rates from standing litter in the field and lab-ratory experiments were calculated according to the followingquation:
T = (dc/dt) × (12 × V × P × T0)(m × V0 × P0 × T)
, (1)
here yT is the CO2 evolution rate at given temperature�g C g−1 dry mass h−1); dc/dt is the slope of the linear regressionor gas concentration gradient through time (ppm C h−1); 12 is thetomic mass of C; m the standing litter mass in jars (g); V is theolume of the jar (L); P is the atmospheric pressure (MPa); T is thebsolute temperature during sampling (K); and V0, P0 and T0 arehe gas mole volume (L), atmospheric pressure (MPa) and absoluteemperature (K) under standard conditions, respectively.
The relationship between CO2 evolution rates from standing lit-er and temperature across −5 to 25 ◦C in laboratory experimentsas described with the following exponential model (Lloyd and
aylor, 1994):
T = B × exp(k × T), (2)
here B and k are the exponential fit parameters. Thereinto, indicates the temperature sensitivity of microbial respiratory.fterwards, we calculated the temperature-adjusted mean dailyespiration rates based on the temperature sensitivity of microbialespiration in the laboratory experiments, daily microbial res-iration measured in the field and daily mean air temperatureKuehn et al., 2004). Especially, the daily maximum respirationates were used to calculate the temperature-adjusted meanourly respiration rates when rain events occurred (Kuehn et al.,004) and lasted more than 2 h. Therefore, annual CO2 flux wasstimated by multiplying the temperature-adjusted mean res-iration rates by standing litter mass (Kuehn et al., 2004). Inhis study, the temperature-adjusted mean respiration rates fromeptember 2011 to January 2012 were calculated through experi-ents conducted in Oct. 2011, from February to May 2012 through
xperiments in April 2012, and from June to August 2012 throughxperiments in July 2012, respectively. In this study, we did notbserved CO2 evolution from standing litter when the incuba-ion temperature was dropped to −12 ◦C (data not shown), andhus did not measure CO2 emission when mean daily temperatureas below −12 ◦C. Furthermore, CO2 evolution rates were roughly
quivalent to half of that at −5 ◦C when the mean daily tempera-ure ranged from −12 to −5 ◦C. Given that mean daily temperaturebove 25 ◦C was relatively scarce (only three days during the exper-mental duration), we regarded that CO2 evolution at mean dailyemperature above 25 ◦C equal to that at 25 ◦C.
.5. Data analyses
All statistical analyses were performed using SPSS 13.0 for Win-ows (SPSS Inc., 2004), and the accepted significance was P = 0.05.ata were tested for normality using the Kolmogorov–Smirnov
est, and all data followed a normal distribution (data not shown).
ne-way analysis of variance (ANOVA) was used to test the effectf the incubation temperature on CO2 evolution rates in laboratoryxperiments, or the effect of the sampling time on CO2 evolutionates and the litter water potential in field experiments. The
ig. 1. Diel changes in CO2 evolution rates from standing-dead D. angustifolia (a–c), aicrovoltmeter (HR-33T) could not operate from 18 to next 6 O’clock at the given
tanding litter was not measured during this period. Means ± SE are shown (n = 5).
orrelation of data collected in field experiments was described byhe Pearson product-moment correlation coefficient.
. Results
.1. Diel pattern of microbial CO2 evolution in the field
Both CO2 evolution rates and the litter water potential variedubstantially with sampling time in each sampling day (all P < 0.01,ppendix Table 1), and showed obvious diel patterns during theampling periods (Fig. 1). In the daytime, litter water potential andO2 evolution rates decreased with increasing air temperature and
ecreasing relative humidity (Fig. 1). At night, CO2 evolution rates
ncreased with rising litter water potential and relative humidity,nd decreasing air temperature (Fig. 1). Rates of CO2 evolutionere highest in the early morning, and lowest in the afternoon
eW
perature and relative humidity (d–f) and litter water potential (h–j). The dew-pointn October 2011 because of low air temperature. Therefore, the water potential of
Fig. 1a–c). Rates of CO2 evolution from standing litter showedtrong positive correlations with relative humidity and litter waterotential, but negatively correlated with air temperature (Table 1).
n summary, daily CO2 evolution rates of standing-dead culmsnd leaves were respectively 6.38 and 40.37 �g C g−1 dry mass d−1
n October 2011, 73.76 and 206.12 �g C g−1 dry mass d−1 in April012, and 148.01 and 741.91 �g C g−1 dry mass d−1 in July 2012.dditionally, significant CO2 evolution occurred even when air
emperature dropped to −4 ◦C in October 2011 (Fig. 1a and d).
.2. Effects of temperature on microbial CO2 evolution in theaboratory
Rates of CO2 evolution from culms and leaves increased withlevating temperature within the range of −5 to 25 ◦C (Fig. 2).ithin the range of 25–35 ◦C, only CO2 evolution rates from culms
Table 1The Pearson correlation coefficients (r) between standing litter-associated microbial respiratory rates and air temperature, relative humidity and standing litter waterpotential in field experiments.
Data Plant organ Air temperature Relative humidity Water potential
October 2011Culms −0.392** 0.604*** 0.566**
Leaves −0.775*** 0.860*** 0.723***
April 2012Culms −0.301* 0.449*** 0.327*
Leaves −0.791*** 0.874*** 0.894***
July 2012Culms −0.751*** 0.638*** 0.871***
Leaves −0.789*** 0.778*** 0.845***
Note:
ilttp
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3
* P < 0.05.** P < 0.01.
*** P < 0.001.
n July 2012 declined with increasing temperature, and CO2 evo-ution rates increased for other treatments (Fig. 2). According to
he exponential models, both culms and leaves CO2 evolution ratesightly correlated with temperature (−5 to 25 ◦C) during the sam-ling periods (all P < 0.001, Fig. 2).
0
25
50
75
100
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October 2011
April 2012
July 2012
October 2011
April 2012
July 2012
CO
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ates
( µg C
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October 2011: yT = 8.762exp(0.077T) (R
2 = 0.950)
April 2012: yT = 8.167exp(0.088T) (R
2 = 0.974)
July 2012: yT = 10.652exp(0.087T) (R
2 = 0.981)
a
Culms
Leaves
b
October 2011: yT = 20.573exp(0.073T) (R
2 = 0.988)
April 2012: yT = 18.141exp(0.078T) (R
2 = 0.953)
July 2012: yT = 21.335exp(0.090T) (R
2 = 0.986)
Temperature (oC)
CO
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tion r
ates
(µg
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Temperature (oC)
October 2011
April 2012
July 2012
CO
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ates
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Temperature (oC)
ig. 2. Microbial CO2 evolution rates from water-saturated culms (a) and leaves (b)f standing-dead D. angustifolia in laboratory experiments. Means ± SE are shownn the inset graphs (n = 5).
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.3. CO2 flux estimate
The estimated CO2 fluxes from standing-dead culms and leavesespectively were 3.07 and 6.81 g C m−2 yr−1, and were equivalento 2.32% and 6.94% of the corresponding annual net production132.30 g C m−2 yr−1 for culms and 98.20 g C m−2 yr−1 for leaves).hereinto, rainfall contributed 0.90 and 1.71 g C m−2 yr−1 to CO2missions from standing-dead culms and leaves, respectively.nnual CO2 flux from standing litter (9.88 g C m−2 yr−1) only con-
ributed to 1.12% of the ecosystem respiration (880 g C m−2 yr−1,ong et al., 2009).
. Discussion
Notably, we found that CO2 evolution from standing litter stillccurred both at −5 ◦C under laboratory conditions and at −4 ◦Cn situ conditions, i.e., standing litter-associated microbial respira-ory activities still occur when temperatures fall below freezing.imilarly, Kuehn et al. (2004) also observed significant CO2 evo-ution from standing litter at temperature approaching freezing,nd inferred that microbially mediated C mineralization of stand-ng litter is widespread in wetlands even in cold climates. Ouresults provide assistant proofs for the generality of standing litter-ssociated microbial respiration in temperate wetlands.
In this study, CO2 flux from standing litter (9.88 g C m−2 yr−1)eld approximately 4.29% of the annual aboveground net pro-uction. Kuehn et al. (2004) also found that about 8.5% of netboveground production was mineralized under standing con-itions in temperate littoral wetlands. Our study implies thaticrobial decay of standing litter is not only an important stage
uring plant litter decomposition, but also an essential process of cycle in the freshwater marsh in the Sanjiang Plain, Northeasthina.
Interestingly, the CO2 flux from standing litter only con-ributed to 1.12% of the ecosystem respiration in this temperatereshwater marsh. However, Kuehn et al. (2004) observed thatO2 flux from standing litter was 93 g C m−2 yr−1 in a Phrag-ites australis-dominated temperate littoral wetland, and occupied
pproximately 10% of ecosystem respiration (919.8 g C m−2 yr−1,oehm, 2005). Moreover, in a Juncus effuses-dominated subtrop-
cal freshwater marsh, Kuehn and Suberkropp (1998b) foundhat the rates of CO2 evolution from standing litter rangedrom 1.37 to 3.35 g C m−2 d−1, and even was far greater thanhe sediment respiration rates (0.12–2.43 g C m−2 d−1, Roden and
etzel, 1996). These inconsistent patterns may be related to
he following reasons. Firstly, net aboveground production inmergent macrophyte-dominated wetlands in the previous stud-es often exceeds 2000 g dry mass m−2 yr−1 (Gessner et al., 1996;
etzel and Howe, 1999; Kuehn et al., 2004), which is far higher
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han that in D. angustifolia-dominated marshes in the Sanjianglain (approximately 480 g dry mass m−2 yr−1). Compared with. angustifolia-dominated marshes in the Sanjiang Plain, a rela-
ive high aboveground plant production in these subtropical andemperate wetlands could result in greater standing litter massnd thus CO2 emission from standing litter. Secondly, the dif-erences in standing litter-associated microbial respiration ratesnfluence the contribution of CO2 fluxes from standing litter to thecosystem respiration. In our study, rates of CO2 evolution frometted D. angustifolia leaves were 54–84 �g C g−1 dry mass h−1 at
5 ◦C under laboratory conditions. However, the mineralizationate of wetted P. australis leaves was 200–240 �g C g−1 ash-freery mass h−1 at the same incubation temperature (Kuehn et al.,004), and maximum microbial respiration rate of standing-deadriglochin maritime leaves even reached 509 �g C g−1 dry mass h−1
Buth and Voesenek, 1988). Moreover, the CO2 evolution fromtanding-dead leaves of common wetland plant species (e.g., Jun-us roemerianus, Limonium vulgare and Spartina anglica) oftenxceeded 100 �g C g−1 dry mass h−1 at temperature below 15 ◦CNewell et al., 1985; Buth and Voesenek, 1988). Thirdly, meannnual air temperature in this study area is 2.5 ◦C, which is obvi-usly far lower than that in most of the subtropical wetlands, andven temperate wetland with the same latitude (e.g., 9 ◦C in theittoral wetland around Lake Neuchâtel in western Switzerland,aberg and Guisan, 2002; 7.9 ◦C in the fen meadows near Zürichn northern Switzerland and 9 ◦C in the fens near Utrecht in cen-ral Netherlands, Güsewell, 2005). In the Sanjiang Plain, a relativeower temperature would suppress CO2 evolution from standingitter. Our results suggest that CO2 emission from standing litterould be ignored in assessing ecosystem C budget in D. angustifolia-ominated temperate wetlands in the Sanjiang Plain, Northeasthina.
. Conclusions
In this study, we investigated the annual CO2 flux from stand-ng litter and assessed its contribution to ecosystem respiration in
D. angustifolia-dominated freshwater marsh in the Sanjiang Plain,ortheast China. CO2 emission from standing litter was detectedhen temperature was below freezing. Standing litter-associatedicrobial respiration accounted for a considerable portion of
boveground production, but only a tiny part of ecosystem res-iration in a D. angustifolia-dominated freshwater marsh in theanjiang Plain. Our results confirm that microbially mediated Cineralization of standing litter is a key component of litter decom-
osition and C cycle in temperate wetlands, and also suggest thatO2 evolution from standing litter could be neglected in develop-
ng C budget in the D. angustifolia-dominated freshwater marshesn the Sanjiang Plain, Northeast China.
cknowledgements
This research was supported by the “Strategic Priority Researchrogram – Climate Change: Carbon Budget and Related Issue” ofhe Chinese Academy of Sciences (Nos. XDA05050508 and Nationalatural Science Foundation of China (Nos. 31100357, 41103037
nd 41171169). We thank Guisheng Yang and Guiqun Li for theeld work and Xiaoyan Zhu for the laboratory analyses, and theditor (Dr. William J. Mitsch) and two anonymous reviewers forheir time and suggestions.
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ppendix A. Supplementary data
Supplementary data associated with this article can beound, in the online version, at http://dx.doi.org/10.1016/j.ecoleng.013.12.002.
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