Response of litter decomposition to simulated N deposition in disturbed,rehabilitated and mature forests in subtropical China

Jiangming Mo1,3, Sandra Brown2, Jinghua Xue1, Yunting Fang1 & Zhian Li11South China Botanical Garden, the Chinese Academy of Sciences, 526070, Dinghu, Zhaoqing, Guangdong,China. 2Winrock International, 1621 N. Kent St., Suite 1200, Arlington, VA, 22209, USA. 3Correspondingauthor*

Received 16 May 2005. Accepted in revised form 23 November 2005

Key words: China, disturbance, forest succession, nitrogen deposition, litter decomposition, response,subtropics

Abstract

The response of decomposition of litter for the dominant tree species in disturbed (pine), rehabilitated (pineand broadleaf mixed) and mature (monsoon evergreen broadleaf) forests in subtropical China to simulatedN deposition was studied to address the following hypothesis: (1) litter decomposition is faster in matureforest (high soil N availability) than in rehabilitated/disturbed forests (low soil N availability); (2) litterdecomposition is stimulated by N addition in rehabilitated and disturbed forests due to their low soil Navailability; (3) N addition has little effect on litter decomposition in mature forest due to its high soil Navailability. The litterbag method (a total of 2880 litterbags) and N treatments: Control-no N addition,Low-N: )5 g N m)2 y)1, Medium-N: )10 g N m)2 y)1, and High-N: )15 g N m)2 y)1, were employed toevaluate decomposition. Results indicated that mature forest, which has likely been N saturated due to bothlong-term high N deposition in the region and the age of the ecosystem, had the highest litter decompo-sition rate, and exhibited no significant positive and even some negative response to nitrogen additions.However, both disturbed and rehabilitated forests, which are still N limited due to previous land usehistory, exhibited slower litter decomposition rates with significant positive effects from nitrogen additions.These results suggest that litter decomposition and its responses to N addition in subtropical forests ofChina vary depending on the nitrogen status of the ecosystem.

Introduction

Atmospheric deposition of nitrogen – specificallyoxides of nitrogen (nitrate and NOx) mainlyfrom fossil fuel emissions and also ammoniumfrom production and use of fertilizers remain ele-vated in industrial regions of the world and areaccelerating in many developing regions (Gallo-way et al., 2003; Matson et al., 1999, 2002). Over40% of all nitrogen fertilizers are now used inthe tropics and subtropics and over 60% will beused there by 2020. At the same time, fossil fuel

use is expected to increase by several hundredpercent in many areas of the tropics over thecoming decades (Hall and Matson, 1999). Con-cern about the ecological effects of elevated Ndeposition on terrestrial ecosystems is currentlyincreasing (Galloway et al., 2003; Magill et al.,2004; Matson et al., 1999; Tietema et al., 1998).Nitrogen additions have been shown to affect awide range of temperate forest ecosystem proper-ties and processes (such as altering net primaryproduction and nutrient cycling of the ecosys-tem), especially when inputs are large and contin-uous (Matson et al., 2002). There is growingevidence that N cycling in tropical environments*E-mail: mojm@scib.ac.cn

Plant and Soil (2006) 282:135–151 � Springer 2006DOI 10.1007/s11104-005-5446-7

is different from temperate systems (Hall andMatson, 2003; Matson et al., 1999, 2002). A fun-damental aspect of this difference is that tropicalforest ecosystems are more often phosphorus (P)limited than N limited (Vitousek and Sanford,1986). Also, many tropical forest soils are highlyacidic, with low base cation concentrations (Mat-son et al., 1999). However, most studies of theconsequences of enhanced nitrogen depositionhave been performed in temperate forest ecosys-tem in which biological processes are often lim-ited by nitrogen supply, little information isavailable about responses to atmospheric nitro-gen deposition in subtropical and tropical forests(Galloway et al., 2003; Matson et al., 1999,2002), especially in the forests of China (Chenet al., 2004).

In China the use and emission of reactive N in-creased from 14 TgN y)1 in 1961 to 68 TgN y)1

in 2000 and is expected to reach 105 TgN y)1 in2030 (Zheng et al., 2002). Currently this leads tohigh atmospheric nitrogen deposition in some for-ests of southern China. For example, the amountof nitrogen deposition from rainfall in a pine for-est of Guangzhou (Guangdong province) was60 kg ha)1 y)1 (Ma, 1989). In a forest of Dinghu-shan Biosphere Reserve, N deposition increasedfrom 36 kg ha)1 y)1 in 1994 to 38 kg ha)1 y)1 in2001 (Huang et al., 1994; Zhou and Yan, 2001),and in Guangzhou city deposition increased from46 kg ha)1 y)1 in 1988 to 73 kg ha)1 y)1 in 1990(Ren et al., 2000). In temperate regions of Europeand North America, forests receiving inorganicnitrogen deposition below 8–10 kg ha)1 y)1 retainall N input. However, above this level of deposi-tion, forests often leach nitrate and the ecosystemwill move towards nitrogen saturation with signifi-cant biological and ecological responses occurring(Aber et al., 1998, 2003; MacDonald et al., 2002).At inputs above 25–30 kg ha)1 y)1, all the studiedforests in Europe were nitrogen saturated (as de-fined in Aber et al., 1998) (MacDonald et al.,2002). With atmospheric nitrogen deposition insome Chinese forests currently exceeding theabove-cited critical values, it is possible that exces-sive nitrogen inputs could saturate the retentioncapacity of Chinese forest ecosystems.

Most of the land originally covered with pri-mary forests in China has been degraded byhuman activities during the past several hundredyears (Wang et al., 1982). In extreme cases, the

land became completely non-vegetated (He andYu, 1984). Currently, Chinese deforestation isestimated to be on the order of 0.61 million haper year during the 1990s and the remnant natu-ral forest area now is less than 9% of total terri-tory (Liu et al., 2000). Attempts to reverse thisprocess of land degradation have been initiatedin the subtropical and tropical region of China.Over the last few decades, large areas have beenreforested with a native species, to prevent fur-ther degradation of the landscape. Cutting of thetrees is now prohibited, but harvesting of under-story and litter is allowed to satisfy human fuelneeds. These rehabilitated forests (reforested butno harvesting) and the disturbed forests covermore than half of the total forest area in sub-tropical and tropical China (Mo et al., 2004).However, the effects of these significant land-usechanges on the ecosystems are poorly known(Mo et al., 2003, 2004).

Nitrogen has long been recognized as animportant factor regulating litter decompositionprocesses in forest ecosystems. However, studieson the effects of addition of N supply on thedecomposition of litter have shown different re-sults, ranging from positive to negative effects onthe decomposition rate. Prescott (1996) reporteda direct relationship between decomposition ratesand the amount of extractable N in the forestfloor. Vestgarden (2001) reported a positive effectof the external N addition on needle litterdecomposition. Other studies showed either no(Prescott et al., 1999; Vitousek, 1998) or depress-ing (Agren et al., 2001 ; Magill and Aber, 1998;Micks et al., 2004) effects of N on litter decom-position rate. A positive response in the initialdecomposition phase and a negative response inlater stages have also been found (Berg et al.,1998; Berg and Matzner, 1997). Thus, to reach abetter understanding of the influence of N on thedecomposition process, there is still a need forfurther investigation (Adams, 2003; Vestgarden,2001). Furthermore, most studies of the effects ofnitrogen addition on litter decomposition havebeen performed in temperate forest ecosystems,little information is available about responses toatmospheric nitrogen deposition in subtropicaland tropical forests (Micks et al., 2004; Vitousek,1998). In addition studies on litter decompositionand its correlation with N availability are mostlyrestricted to ecosystems limited in N availability

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(Berg, 1988; Koopmans et al., 1998; Micks et al.,2004; Tietema, 1998).

The effects of nitrogen saturation and landuse are likely to cause significant changes in litterdecomposition, a key process affecting soil fertil-ity, nutrient cycling and primary productivity ofecosystems. It is therefore critical to address andpredict the effects of increasing deposition ofnitrogen and the effects of land use change onlitter decomposition of forests in China, espe-cially in southern China where industry and agri-culture has recently been increasing rapidly. Inthis paper we report on a study designed todetermine the effects of simulated N depositionon the decomposition of litter for the major treespecies of Dinghushan forests in subtropical Chi-na. It is proposed that adding N to the soil-litterof N limited ecosystem should increase microbialactivity, but any increase in available N shouldnot affect microbial activity in N saturated eco-system (Berg, 1986, 1998; Berg and Matzner,1997). The objective of this study was to test thefollowing hypothesis: (1) litter decomposition isfaster in mature forest than in rehabilitated/dis-turbed forests; (2) litter decomposition is stimu-lated by N addition in rehabilitated anddisturbed forests due to their low soil N avail-ability; (3) N addition has little effect on litterdecomposition in mature forest due to its highsoil N availability.

Methods

Site description

This study was conducted in the Dinghushan Bio-sphere Reserve (DHSBR). The reserve lies in themiddle part of Guangdong Province in southernChina (112�10¢ E longitude and 23�10¢ N lati-tude) and occupies an area of approximately1200 ha. In the reserve, we have established threeresearch sites comprising different stages of forestsuccession: the monsoon evergreen broadleaf for-est (mature), mixed pine and broadleaf forest(rehabilitated) and pine forest (disturbed). Themonsoon evergreen broadleaf forest, at about250–300 m above sea level (asl) occupies 20% ofthe reserve area, the mixed pine and broadleafforest, at about 200 m asl occupies 50%, and thepine forest, at about 50–200 m asl occupies 20%

(Zhou et al., 1986). Monks in the temples haveprotected the monsoon evergreen broadleaf fromhuman impacts for more than 400 years. Thepine-broadleaf mixed forest (rehabilitated) origi-nated from a planted pine forest that was natu-rally invaded and colonized by broadleaf speciesand is a transitional forest from pine to monsoonevergreen broadleaf forest. The age of rehabili-tated forest is about 65 years (Wang et al., 1982).It is relatively inaccessible to the rural popula-tion, and litter and understory harvesting havebeen minimal to absent. The pine forest (dis-turbed) was planted in about 1930. It has beenunder constant human pressures most of the timesince it was planted (generally the harvesting ofunderstory and litter). The original site of bothrehabilitated and disturbed forests was badly ero-ded and degraded (Mo et al., 1995; Wang et al.,1982). Thus, these forests vary both in level ofhuman impacts as well as stages of succession,site conditions, and species assemblages (Moet al., 2003; Wang et al., 1982).

The reserve has a monsoon climate and is lo-cated in a subtropical moist forest life zone (sen-su Holdridge, 1967). The mean annual rainfall of1927 mm has a distinct seasonal pattern, with 75percent of it falling from March to August andonly 6 percent from December to February (Hu-ang and Fan, 1982). Annual average relativehumidity is 80%. Mean annual temperature is21.0 �C, with an average temperature of the cold-est (January) and hottest (July) month of 12.6 �Cand 28.0 �C, respectively. The soils in the threestudy sites are lateritic red earth formed fromsandstone with variable soil depths. In the ma-ture forest, the soil is deeper than 60 cm. In therehabilitated forest, depth ranges from 30 to60 cm, and in the disturbed forest the depth isgenerally less than 30 cm to bedrock (Brownet al., 1995).

The major species in mature forest are Castan-opsis chinensis Hance, Schima superba Chardn. &Champ., Cryptocarya chinensis (Hance) Hemsl.,Cryptocarya concinna Hance, Machilus chinensis(Champ. Ex Benth.) Hemsl., Syzygium rehderia-num Merr. & Perry in the tree layer and Calamusrhabdicladus Burret, Ardisia quinquegona Bl. andHemigramma decurrens (Hook.) Copel.in theunderstory layers (Wang et al., 1982). Treeheights range from 4 to 30 m and diameters from5 to 163 cm (Wang et al., 1982). The major

137

species in rehabilitated forest are Pinus massoni-ana Lamb, Schima superba, Castanopsis chinensis,Craibiodendron kwangtungense S. Y. Hu, Linderametcalfiana Allen, Cryptocarya concinna in thetree layer and Rhodomyrtus tomentosa (Ait.)Hassk, Evodia lepta (Spreng.) Merr. in the under-story (Wang et al., 1982). Tree heights range from4 to 12 m and diameters from 4 to 48 cm (Wanget al., 1982). Disturbed forest is dominated byPinus massoniana. Pine trees range from 100 to1000 trees ha)1, with diameters of 4–32 cm andheights of 3–11 m (Brown et al., 1995). Age ofpine trees range from 12 to 69 years, with a meanvalue of 30 years. Understory species includedgrasses, ferns, vines and shrubs for a total of 43species (Brown et al., 1995). The disturbed forestis subject to human impact of harvesting litterand understory by local people. The harvestingaccording local practice occurred about 2–3 timesa year (Brown et al., 1995).

Total leaf litter of the studied forests wasmainly contributed by the dominant tree specieswith variations among forest types (Zhang et al.,2000). In mature forest, Castanopsis chinensiscontributed greatest amount of leaf litter to thetotal leaf litter (40% of total leaf litter), followedby Cryptocarya chinensis (12%), Syzygium rehde-rianum (6%) and Machilus chinensis (5%). Inrehabilitated forest, Pinus massoniana contributed31% of total leaf litter, similarly Schima superbacontributed 30% of total leaf litter. In disturbedforest, however, much higher proportion of totalleaf litter was contributed by Pinus massoniana(91%). Thus sampling of leaf litter from the se-lected species as done in this litter decompositionstudy is representative the studied forests.

Soil properties were measured using the sam-ples collected in July 2004. The results are similarto those reported for these forest types by Moet al. (2003), and showed that the mature foresthad higher total C, total N and available P, butlower soil pH, C/N ratio and soil bulk density

than disturbed and rehabilitated forests(Table 1).

Experimental treatments

Nitrogen addition experiments were initiated with-in each of the three forest types in 2003. Four Naddition treatments (in three replicates) wereestablished in mature forest: Control (without Nadded), Low-N (5 g N m)2 y)1), Medium-N(10 g N m)2 y)1) and High-N (15 g N m)2 y)1),but only three treatments were established in reha-bilitated and disturbed forests (Control, Low-Nand Medium-N). Thirty plots of dimensions 20mby 10m were established )12 in mature, 9 in reha-bilitated and 9 in disturbed forest, – surroundedby a 10 m wide buffer strip. All plots and treat-ments were laid out randomly. NH4NO3 solutionwas sprayed monthly by hand onto the floor ofthese plots as 12 equal application over the wholeyear and beginning in July 2003. Fertilizer wasweighed, mixed with 20 L of water, and applied tothe plots using a backpack sprayer below the can-opy. Two passes were made across each plot to en-sure an even distribution of fertilizer. The Controlplots received 20 L water without N added.

Field sampling

Litter decomposition was determined by placingfresh litter in mesh bags in the plots. Leaf litterwas collected using litter traps and nylon meshplaced on the forest floor under the trees of se-lected species in the study sites during Marchand June 2003, the season of peak litterfall(Zhang et al., 2000). The selected trees were alsoshaken as needed. All the leaves were air-dried toa constant weight. The leaves of an individualspecies were mixed to obtain a uniform mixturebefore filling the mesh bags. Six sub-samples(about 10.00 gram per sub-sample) from eachspecies were analyzed for the initial oven-dry

Table 1. Mineral soil properties (0~10 cm depth) of the control plots in disturbed, rehabilitated and mature forests in subtropicalChina (mean, SE in parentheses; n=3 for all samples; measured in July 2004)

Forests pH (H2O) Total C(mg g)1)

Total N(mg g)1)

C/N Available P(mg kg)1)

Soil bulkdensity (g cm)3)

Disturbed (pine) 3.93(0.08) 22.7(3.1) 1.3(0.1) 17.01(1.35) 3.59(0.28) 1.16(0.05)

Rehabilitated (mixed) 3.91(0.03) 17.3(1.2) 1.2(0.1) 14.39(1.03) 4.21(0.30) 1.22(0.01)

Mature 3.76(0.01) 32.1(2.7) 2.5(0.2) 12.84(2.27) 4.96(0.16) 0.98(0.06)

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weight (conversion rate from 40 to 105 �C), andinitial N and P concentrations. A total of 2880litter bags were prepared from mesh (0.5 mm inthe bottom and 2 mm in the top) polyvinylscreen of approximately 25 cm�25 cm in dimen-sion at the beginning of the study (June 2003).The number and contents of the bags were asfollows: 1800 bags for mature forest (300 bagsfor each species and for mixed litter; leaf litterfrom the four dominant tree species: Castanopsischinensis, Syzygium rehderianum, Machilus chin-ensis, Cryptocarya chinensis, and mixed litter(mixed about one fourth of leaf litter for eachspecies)), 810 bags for rehabilitated forest (270bags for each species and for mixed litter; leaf lit-ter/needles are two dominant tree species: Pinusmassoniana, Schima superba, and mixed litter(needle plus leaf litter of Schima superba, mixedabout half and half )), and 270 bags for dis-turbed forest (needle of Pinus massoniana). Eachbag was filled with about 10.00 g, air-dried mass,of litter. At the end of June 2003, these litterbags were evenly distributed among each plot.

Five litter bags for each species or for eachmixed litter (a total of 480 bags at each collec-tion: 300 bags for mature, 135 bags for rehabili-tated and 45 bags for disturbed forests) werecollected from each plot (a total of 30 plots: 12in mature, 9 in rehabilitated and 9 in disturbedforests) at about 3, 6, 9, 12, and 18 months afterthe start of the study (July 2003), yielding a sam-ple size of 15 for each species and each N treat-ment. The bags were returned to the lab forseparation and analysis.

Mineral soils (0~10 cm) were sampled approx-imately 25 days after each N application todetermine soil extractable NHþ4 -N and NO�3 . Ineach plot, 15 soil cores (2.5 cm in diameter) werecollected randomly and composited into onesample (a total of 30 samples in each collection).KCl extractable NHþ4 -N and NO�3 -N were ana-lyzed back in the lab.

Laboratory procedures and data analyses

In the laboratory, ingrown roots, if any, wereremoved from the bags, brushed free of foreignmaterials, and oven-dried in paper bags to aconstant weight at 40 �C. After drying, each bagwas weighed individually (Sundarapandian andSwamy, 1999).

Initial N concentration of litter for decompo-sition was determined with semimicro-Kjeldahldigestion (Bremner and Mulvaney, 1982) fol-lowed by detection of ammonium with a Wescanammonia analyzer (Scott et al., 1989), while totalP concentration was analyzed colorimetrically(Anderson and Ingram, 1989).

Soils were sieved (2 mm) and mixed thor-oughly by hand. One 10 g sub-sample from eachcomposite sample was shaken for 1 hour in50 mL 2 mol L)1 KCl, and filtered through pre-leached Whatman no.1 filters, and then frozenimmediately for later analysis. Extract NHþ4 -Nwas determined by the indophenol blue methodfollowed by colorimetry. NO�3 -N was deter-mined after cadmium reduction to NO�2 -N, fol-lowed by sulfanilamide-NAD reaction (Liu et al.,1996).

Subsamples of litter and soil materials weredried to 105 �C, and all results are reported on105 �C basis.

The model for constant potential mass loss(Olson, 1963) is represented by the followingequation:

X=Xo ¼ e�kt

where X/Xo is fraction mass remaining at time t,X the mass remaining at time t, Xo the originalmass, ��e�� the base of natural logarithm, k thedecomposition coefficient, and t the time. Theexponential model was fit to the data using leastsquares regression of the natural logarithm ofmean fraction mass remaining (Kuperman,1999). Half-lives (t0.5) of decomposing litter sam-ples were estimated from k values using the fol-lowing equation (Bockheim et al., 1991):

t0:5 ¼ lnð0:05Þ=ð�kÞ ¼ 0:693=ð�kÞ

A double-exponential function was also used to fitthe data for the species/litter type in which the Naddition had a negative effect in the late stages ofdecomposition: X=Xo ¼ ae�kat þ be�kbt, where kais the rate constant for late stage of decompositionprocess, ��a�� is the proportion of mass loss by thelate stage process, kb is the rate constant for earlystage of decomposition process, ��b�� is the propor-tion of mass loss by early stage process (Berntsonand Aber, 2000).

One-way ANOVA with Tukey’s HSD test wasperformed to test the difference in decomposition

139

rate (values of X/Xo and k) among forests andN treatments for each sample date (Koopmanset al., 1998; Prescott et al., 1992; Ribeiro et al.,2002). For litter decomposition, with samplescollected and analyzed continuously throughoutthe study period, a repeated measure ANOVAwith Tukey’s HSD test was also performed toexamine the difference in decomposition rate(values of X/Xo) among N treatment effects,forest types and litter types. These two statisti-cal methods were also performed for soilextractable NHþ4 -N and NO�3 -N. Residualplots were examined to check equal varianceassumptions for ANOVA and identify statisticaldata outliers. Outliers were removed from allstatistical analyses but included in the figuresand tables. All analyses were conducted usingSPSS 10.0 for windows. Statistical significantdifferences were set with P values <0.05 unlessotherwise stated.

Results

Patterns of leaf litter decomposition in controlplots

The initial average N concentration in the leaflitter of selected dominant tree species was(mg g)1) Castanopsis chinensis 14.0, Syzygium re-hderianum 13.2, Machilus chinensis 16.5, Crypto-carya chinensis 19.0, Schima superba 15.6, Pinusmassoniana 12.8 for rehabilitated forest and 12.2for disturbed forest. In mixed litter it was 15.7for mature forest and 14.2 for rehabilitated for-est. The initial average P concentration in theleaf litter of selected dominant tree species was(mg g)1) Castanopsis chinensis 0.69, Syzygium re-hderianum 0.54, Machilus chinensis 0.74, Crypto-carya chinensis 0.71, Schima superba 0.61, Pinusmassoniana 0.81 for rehabilitated forest and0.65 for disturbed forest. In mixed litter it was0.66 for mature forest and 0.71 for rehabilitatedforest.

Patterns of leaf litter decomposition in con-trol plots reflect the natural process withoutnitrogen additions (Figure 1). The mass remain-ing in litter bags decreased exponentially withtime and was characterized by an initial fasterrate of disappearance, followed by a subsequentslower rate for all species and forests. The regres-

sion equations describing decomposition ratesover time were significant (P<0.05) for all spe-cies and forests (coefficients of determination (r2)varied from 0.67 to 0.99, most of the valuesexceeding 0.88) (Table 2).

Decomposition rates varied depending on for-est, species and the length of exposure of plantlitter on the forest floor (Figure 1). Leaf litterdecomposition was significantly faster in matureforest than in rehabilitated or disturbed forestsfor all sampling dates (P<0.05). However, nosignificant difference in decomposition rate wasfound between rehabilitated forest and disturbedforest for all sampling dates except for the firstperiod. Repeated ANOVA with Tukey’s HSDtest also showed statistically significant differencein mass remaining between mature rehabilitated/disturbed (P<0.001), but not significant betweenrehabilitated forest and disturbed forest over theentire study period. The average decompositioncoefficients for all species (k) for mature, rehabili-tated and disturbed forests were 2.21±0.38,0.28±0.03 and 0.27, respectively (Table 2). Meandecomposition coefficient in mature forest wassignificantly higher than the mean value in reha-bilitated forest (P<0.009) and the mean value ofrehabilitated combined with disturbed forest(P<0.003). At the end of the experiment largedifferences in the mass remaining were found:about 5 percent in mature forest, 64 percent inrehabilitated forest, and 66 percent in disturbedforest. In mature forest, half-lives (t0.5) of litterfor all species varied from 3 to 7 months. Inrehabilitated and disturbed forests, half-lives(t0.5) were within 27–38 months (Table 2).

Decomposition rates also varied by species(Figure 1, Table 2). Repeated ANOVA showedstatistical significant difference in mass remainingamong species over the entire study period(P<0.001). At the end of the experiment, Machi-lus chinensis and Castanopsis chinensis in matureforest showed the fastest rate of mass loss withdecomposition coefficients of 3.08 and 3.05,respectively. Pinus massoniana in disturbed forestshowed the lowest rate of mass loss with decom-position coefficient of 0.27.

Decomposition coefficients (k) were negativelycorrelated (P<0.05) with the corresponding ini-tial litter N/P ratio in mature forest (Figure 2),however, the initial litter N and P concentrationdid not influence their decomposition coefficients.

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Figure 1. Changes of mass loss in decomposing litter for the selected dominant tree species in disturbed, rehabilitated and matureforests of subtropical China. Asterisk (*) indicates significant different at least between two treatments at P<0.05 (n=15).

141

Table

2.Leaflitter

decompositioncoeffi

cient(k)fortheselected

dominanttree

speciesin

disturbed,rehabilitatedandmature

forestsofsubtropicalChina

Forest

type

Species/litter

type

kr2

(month)

Control

Low-N

Medium

-NHigh-N

Control

Low-N

Medium

-NHigh-N

Control

Low-N

Medium

-NHigh-N

Mature

Syzygium

rehderianum

1.72

1.44

1.41

1.32

0.91

0.90

0.78

0.76

4.8

5.8

5.9

6.3

Cryptocaryachinensis

1.12

1.16

0.84

0.84

0.86

0.90

0.88

0.86

7.4

7.2

9.9

9.9

Mixed

litter

2.08

0.84

1.59

1.23

0.92

0.89

0.98

0.91

4.0

9.9

5.2

6.8

Machiluschinenesis

3.08

1.34

0.94

0.62

0.99

0.94

0.85

0.60

2.7

6.2

8.8

13.4

Castanopsischinensis

3.05

1.76

2.58

2.56

0.85

0.90

0.79

0.76

2.7

4.7

3.2

3.2

Mean

2.21

1.31

1.47

1.31

0.91

0.91

0.86

0.78

4.3

6.8

6.6

7.9

SE

0.38

0.15

0.31

0.34

0.03

0.01

0.04

0.05

0.9

0.9

1.2

1.7

Rehabilitated

Pinusmassoniana

0.31

0.40

0.26

0.88

0.97

0.68

26.8

20.8

32.0

Schim

asuperbe

0.29

0.40

0.28

0.79

0.94

0.78

28.7

20.8

29.7

Mixed

litter

0.22

0.30

0.31

0.67

0.76

0.78

37.8

27.7

26.8

Mean

0.27

0.37

0.28

0.78

0.89

0.75

19.7

15.4

19.3

SE

0.03

0.03

0.01

0.06

0.07

0.03

7.2

5.0

6.4

Disturbed

Pinusmassoniana

0.27

0.29

0.30

0.72

0.81

0.79

30.8

28.7

27.7

Note:Decompositioncoeffi

cients

(k)andcoeffi

cients

ofdetermination(r2)are

basedonasingle

negativeexponentialmodel.

Theregressiondescribingdecompositionrate

over

timeissignificantatP<

0.05levelforallspeciesandN

treatm

entsexceptforMachiluschinensisatHigh-N

treatm

ent(r2=

0.62,

P=

0.069).

142

Soil available nitrogen

Soil extractable inorganic N ( NHþ4 -N + NO�3 -N upper 10 cm soil) in the Control plots varieddepending on forest types and sampling dates(Figure 3). In disturbed forest, concentrations ofsoil extractable inorganic N varied from 4.2 to9.9 mg kg)1, with a mean of 5.9 mg kg)1. Com-parable N concentrations were also observed inthe rehabilitated forest (2.2–15.8 mg kg)1, with amean of 6.4 mg kg)1). Much higher concentra-tions of soil inorganic N, however, were found in

mature forest (4.6–27.9 mg kg)1, with an averageof 14.9 mg kg)1). Furthermore, mature foresthad a much higher proportion of NO�3 -N (onaverage 75.8%) than disturbed and rehabilitatedforests (43.6 and 43.2%, respectively).

Soil extractable inorganic N concentrationsresponded to N addition in all forest types, butdiffered between forests and components of inor-ganic N (Figure 3). In disturbed forest, concen-trations of soil extractable NHþ4 -N and NO�3 -Nwere significantly increased by experimental Naddition on several sample dates (Figure 3a–b).Repeated ANOVA, however, showed no statisti-cal significant difference among treatments overthe entire study period (P=0.089 for NHþ4 -N,and P=0.078 for NO�3 -N), due to concentrationfluctuations both between sampling dates and be-tween treatments (Figure 3a–b). There weretrends, however, indicating N additions had in-creased both NHþ4 -N and NO�3 -N concentra-tions in the soil. Average concentrations for the10 samplings in the Control, Low-N and Med-ium-N plots were 3.34, 3.37, and 4.58 mg kg)1

for NHþ4 -N, and 2.60, 5.73 and 4.92 mg kg)1 forNO�3 -N, respectively.

In rehabilitated forest, concentrations of soilextractable NHþ4 -N and NO�3 -N were also sig-nificantly increased by experimental N additionon several sample dates (Figure 3c–d), but werefound to have no statistical significant differenceover the whole year (P=0.162 for NHþ4 -N, andP=0.737 for NO�3 -N, respectively). AverageNHþ4 -N concentration was 3.38, 3.61, and5.10 mg kg)1 and average NO�3 -N concentrationwas 3.03, 3.33 and 3.64 mg kg)1 in the Control,Low-N, and Medium-N treatments, respectively.Similar to those in disturbed and rehabilitatedforests, concentrations of both NHþ4 -N andNO�3 -N in mature forest were significantly in-creased by N addition on several sample dates(Figure 3e–f). Repeated ANOVA showed no sig-nificant difference between N treatments forNO�3 -N (P=0.644), but significant for NHþ4 -N(P=0.009). Concentrations of NO�3 -N in matureforest, however, were 4–5 times higher than indisturbed and rehabilitated forests, with averages12.73, 12.68, 13.18 and 15.10 mg kg)1 in theControl, Low-N, Medium-N, and High-N plotsrespectively. Average NHþ4 -N concentrationswere 2.10, 2.76, 3.08 and 3.71 mg kg)1, respec-tively.

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Figure 2. Relationship of decomposition coefficients (k) andtheir corresponding initial litter nutrient index (N, P and N/Pratio) for the selected dominant tree species in mature forestof subtropical China.

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Responses of leaf litter decomposition to simulatednitrogen deposition

In disturbed forest, decomposition rate increasedslightly with increasing nitrogen treatment levels

(decomposition coefficient (k): medium(0.30)>low (0.29)>control (0.27), Table 2). Re-peated ANOVA, however, showed no statisticallysignificant difference among treatments over theentire study period due to the variation of

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Figure 3. Soil extractable NHþ4 -N and NO�3 -N concentrations in the upper 10 cm mineral soils of disturbed (a, b), rehabilitated(c, d) and mature forests (e, f) of subtropical China. Samples in the disturbed forest were not taken in time for August 2003 owingto high rainfall event. Asterisk (*) indicates significant different at least between two treatments at P<0.05 (n=3). The scale aty-axis in (f) was doubled to show some high NO�3 -N data in the mature forest.

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decomposition rates both between sampling datesand between treatments. However, the effect ofnitrogen addition on pine needle decompositionvaried depending on the length of its exposure.After three months, there was a significant differ-ence in decomposition rate between control andlow/medium plots (P<0.05, Figure 1), but nosuch significant difference was found betweentreatments in the remaining sampling dates (Fig-ure 1).

In rehabilitated forest, mean decompositioncoefficients were low (0.37)>medium (0.28)>control (0.27), the difference between low andcontrol was significant (P<0.05) (Table 2). Theeffect of nitrogen addition varied depending onlitter type, nitrogen treatment level and thelength of exposure. Results of repeated ANOVAindicated that there was no significant overallnitrogen effect on decomposition rates for anyspecies (litter type) except for mixed litter. Re-peated ANOVA with Tukey’s HSD test showedthat decomposition of mixed litter was signifi-cantly faster in N treated plots (low/medium)than in control plots (P<0.05). However, one-way ANOVA with Tukey’s HSD test showedthat, for both pine and Schima superba, lownitrogen treatment significantly increased decom-position rate for all sampling dates (P<0.05)beyond the first three (Figure 1), but mediumnitrogen addition had no such effect on any sam-pling dates for Schima superba and only signifi-cantly on the second sampling date for pineneedle (P<0.05) (Figure 1). The effect of nitro-gen addition on mixed litter was more pro-nounced than on pine needles or leaf litter ofSchima superba. Decomposition coefficient formixed litter increased with nitrogen treated lev-els: medium (0.31)>low (0.29)>control (0.22)(Table 2). Both low and medium nitrogen treat-ments were found to significantly increase mixedlitter decomposition rate for all sampling dates(P<0.05) beyond the first two (Figure 1).

In mature forest, no significant positive effect(increase litter decomposition rate) was found forany species and for any nitrogen treatment levels.Instead, some significant negative effects (de-crease litter decomposition rate) of nitrogen addi-tion were found for all species (p < 0.05) exceptfor Castanopsis chinensis and Cryptocarya chinen-sis (Figure 1). Mean decomposition coefficientsfor all species was: control (2.21)>medium

(1.47)>low (1.31)=high (1.31) (Table 2). The ef-fect of nitrogen addition also varied dependingon litter type, treatment level and the length ofexposure (Figure 1). Results of repeated ANO-VA indicated that there was a statistically signifi-cant difference in decomposition rate amongtreatments over the entire study period for all lit-ter types except for Cryptocarya chinensis andCastanopsis chinensis. Repeated ANOVA withTukey’s HSD test showed that decompositionrate was significantly lower in high N plots thanin control plots for mixed litter, lower in all Ntreated plots than in control plots for Machiluschinensis and lower in low/high plots than incontrol plots for Syzygium rehderianum(P<0.05). However, one-way ANOVA with Tu-key’s HSD test showed that, in comparison withthe decomposition rate in control plots, lownitrogen treatment was found to significantly re-duce decomposition rate on the first and fourthsampling dates for Syzygium rehderianum(P<0.05), and on the last sampling date formixed litter (P<0.05). All nitrogen treatmentlevels were found to significantly reduce decom-position rate on the last three sampling dates forMachilus chinensis (P<0.05, Figure 1).

This negative effect of N addition in the latestage of decomposition was also confirmed bythe results of the analysis with double exponen-tial model fitting for Machilus chinensis andmixed litter (Table 3). For example, rate con-stants in control, low, medium and high N plotsin the early stage of decomposition process forMachilus chinensis were (kb): 2.62, 0.53, )0.16and 3.40, respectively, but in the later stage ofdecomposition the rate constants were (ka): 2.62,2.11, 2.45 and )0.31, respectively. However,there was no such difference between rate con-stants among treatments (kb values ranged from101.00 to 101.02) for the remaining species in thelater stage of decomposition.

Discussion

Rates of decomposition of litter in control plotsof mature forest were high in comparison withthe values reported for temperate ecosystem andwere similar to those for tropical ecosystems.Melillo et al. (1982) reported that decompositioncoefficients of temperate hardwood species

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ranged from 0.08 to 0.47. Stohlgren (1988) alsoreported that decomposition coefficients of sixspecies in a temperate forest varied from 0.18 to0.62. In a subtropical evergreen broad-leaved for-est of Japan, decomposition coefficients variedfrom 0.66 to 1.19 (Alhamd et al., 2004). In atropical dry secondary forest of Mexico, decom-position coefficients ranged from 1.46 to 2.54,with a mean of 1.92 (Xuluc-Tolose et al., 2003).In semi-evergreen tropical forests, decompositioncoefficients ranged from 0.41 to 2.39 (Lorangeret al., 2002). Takeda (1996) reported that themean value of decomposition coefficients fortropical forests was 1.85. Half-lives of litter forall species in mature forest varied from 3 to7 months and were slightly longer than the val-ues (from 1.72 to 5.10 months) found in a tropi-cal forest of India (Sundarapandian and Swamy,1999).

Contrary to those in mature forest, decompo-sition rates in rehabilitated and disturbed forestswere low in comparison with values reported fortemperate and tropical forests. Decomposition

coefficients for litter typical of these two forestswere lower than the values reported above fortemperate and tropical forests, lower than thevalues (0.31–0.46) compiled from the availableliterature on different temperate pine species lit-ter decomposition by Das and Ramakrishnan(1985), and also lower than the values for othertropical and subtropical humid broadleaf andpine forests (1.0–1.75; Brown and Lugo, 1982;Cuevas et al., 1991).

In sum, litter decomposition rates (includingmixed litter) in control plots was significantly fas-ter in mature forest than in rehabilitated or dis-turbed forests. This result indicates thatsuccessional stage, and corresponding speciesmix, has a significant effect on litter decomposi-tion. This result is supported by the suggestionthat old-growth forest is more efficient in therecycling of nutrients (Brown and Lugo, 1990).

The reason for higher decomposition rate inmature forest than in rehabilitated and disturbedforests can be explained by the difference in sitecondition (environment) and plant species

Table 3. Parameters for the double exponential model fitting decomposition process of leaf litter for the selected dominant treespecies in mature forest of subtropical China

Species/litter type Treatment Factor r2

A b ka kb

Syzygium rehderianum Control 0.36 0.64 101.02 1.03 0.96

Low-N )0.13 1.13 101.00 1.20 0.97

Medium-N 0.37 0.63 101.00 0.72 0.89

High-N 0.22 0.78 101.00 0.68 0.82

Cryptocarya chinensis Control 0.12 0.88 101.00 0.78 0.91

Low-N )0.15 1.15 101.00 1.25 0.91

Medium-N 0.32 0.68 101.00 0.67 0.97

High-N 0.08 0.92 101.00 0.65 0.91

Mixed litter Control 0.23 0.77 5.84 1.45 0.98

Low-N 0.42 0.58 7.68 0.52 0.99

Medium-N 0.12 0.89 0.45 2.11 0.98

High-N 0.87 0.13 0.90 108.00 0.95

Machilus chinensis Control 0.40 0.62 2.62 2.62 0.99

Low-N 0.78 0.24 2.11 0.53 0.96

Medium-N 0.84 0.17 2.45 )0.16 0.98

High-N 0.23 0.78 )0.31 3.40 0.99

Castanopsis chinensis Control 0.47 0.53 101.00 1.39 0.97

Low-N )0.05 1.05 101.00 2.72 0.99

Medium-N 0.61 0.39 101.00 0.89 0.97

High-N 0.61 0.39 101.00 0.76 0.94

Note: factor and coefficients of determination (r2) are based on a binomial exponential model; The regression describing decompositionrate over time is significant at P<0.01 level for all species/litter type and N treatments.

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(Xuluc-Tolosa et al., 2003). It is generally acceptedthat litter decomposition is faster in nutrient-richsites than in nutrient-poor sites (Hobbie, 2000;Vitousek, 1998) and that litter with high initialnitrogen concentration exhibits relatively fasterdecomposition (Berg and Matzner, 1997; Fog,1988; Singh and Gupta, 1977; Sundarapandianand Swamy, 1999; Xuluc-Tolose et al., 2003). Asmentioned above, the mature forest has been pro-tected from human impacts for more than400 years and is the representative forest (mon-soon evergreen broadleaf forest) of the lower sub-tropics in China. However, the original site ofboth rehabilitated and disturbed forests was badlyeroded and degraded (Brown et al., 1995; Moet al., 1995; Wang et al., 1982). The side conditionfor microbial activity is likely better in mature for-est than in rehabilitated or disturbed forests. Forexample, the quantity of soil microbial biomasswas found to be highest in mature forest, followedby rehabilitated and disturbed (Fu et al., 1995; Yiet al., 2002). Moreover, the soil availablephosphorus was mature>rehabilitated>dis-turbed (forest), the soil nitrogen content wasmature>disturbed>rehabilitated (forest), and thesoil C/N ratio was disturbed > rehabilitated >mature (forest) (Table 1; also see Table in Moet al., 2003). The initial average N concentrationin the leaf litter of selected tree species was highestin mature forest (15.7 mg g)1), followed by reha-bilitated (14.2 mg g)1) and disturbed forest(12.2 mg g)1). It has also been found that matureforest has higher soil water storage capacity thanrehabilitated and disturbed forests (Zhang andZhuo, 1989).

As reported, the disturbed forest has been un-der constant human pressures since it was plan-ted in 1930. The disturbance was generally theharvesting of understory and litter (about 2–3times a year, Brown et al., 1995; Mo et al.,1995). This harvesting practice not only removesthe nutrients therein, but it also removes organicmatter and, thus, substrate for microbial activity,resulting in higher nitrogen leaching losses. As aresult, the site productivity and nitrogen levelwas low (Brown et al., 1995; Mo et al., 1995,2003, 2004). Similarly, the rehabilitated forest,originating from a planted pine forest that wasnaturally invaded and colonized by broadleafspecies, has not fully recovered its soil nutrientavailability during the past several decades, and

its soil nitrogen availability was also low (seeFigure 3, Table 1; Mo et al., 2003, 2004). It islikely that nitrogen availability is one of the ma-jor factors limiting litter decomposition in bothrehabilitated and disturbed forests. This is par-tially supported by results of a separate litterdecomposition experiment in disturbed forests(Mo et al., 1995), in which pine needles immobi-lized nitrogen during the first 200–250 days ofdecomposition, indicating that pine needles con-tained insufficient nitrogen to support microbialuse of the carbon in disturbed forest (Mo et al.,1995). Results from this study also confirmedthat soil nitrogen was limiting factor for litterdecomposition in both rehabilitated and dis-turbed forests. Thus, we believed that disturbedand rehabilitated forests are still N limited. Ourresult is also consistent with that reported byTietema et al. (1998) for a coniferous forest withsimilar soils characteristics.

The addition of exogenous nitrogen to thesoil-litter subsystem has been reported to consid-erably alter the rate of litter decomposition. Pres-cott (1996) reported a direct relationship betweendecomposition rates and the amount of extract-able N in the forest floor. Decomposition ratesincreased along the gradient of increasing atmo-spheric N deposition (Kuperman, 1999). The in-crease in decomposition rate caused by nitrogenaddition were also reported by several authors(Boxman et al., 1995; Entry and Backman, 1995;French, 1988; Hunt et al., 1988; Vestgarden,2001) and were consistent with results found inrehabilitated and disturbed forests of our study.At elevated atmospheric N inputs, increased ratesof litter decomposition have been attributed toimproved litter quality (Koopmans et al., 1998).Kuperman (1999) attributed these positive effectsto the increasing available exogenous nitrogenpools that would lower the substrate C-to-Nratios available to decomposers during litterdecomposition. This hypothesis was supportedby the highly significant relationship between theC-to-N ratio and percent mass remaining foundin his study. Aerts et al. (1995) found the sametrend that the C-to-N ratio of leaf litter wasreduced and decomposition rates increased uponenhanced nitrogen supply.

The results of nitrogen additions in themature forest show a different trend. No positiveeffects and even some negative effects of nitrogen

147

addition on litter decomposition were found forsome species in mature forest (Figure 1). Theseresults were similar to those found in a subhumidtropical forest, where the higher the total N oflitter, the less likely there would be significant ef-fects of addition of N on decomposition (Kwab-iah et al., 1999), and similar to the result foundin a Metrosideros plolymorpha dominated Hawai-ian forest, where N addition had little or no sig-nificant positive effect on decomposition of litter(Vitousek, 1998). The negative effects were alsosimilar to those found in a long-term litter bagstudy, in which N addition was found to signifi-cantly decrease the rate of mass loss of litter(Agren et al., 2001 ; Magill and Aber, 1998;Prescott et al., 1999) and to the results found ina NH4NO3 addition experiment in an oak forestand a red pine plantation (Micks et al., 2004).Our results supported the conclusion by Fog(1988), that N addition generally has either noeffect or a negative effect on decomposition.

The reasons for our results may be explainedby the followings. First, mature forest is likely Nsaturated. Soil available N was higher in matureforest than in disturbed and rehabilitated forests.In the control plots of mature forest, mean con-centration of extractable inorganic N was twiceas high as that in control plots of disturbed andrehabilitated forests. The mature forest had ahigher proportion of NO�3 -N among extractableinorganic N in comparison to those in disturbedand rehabilitated forests. Higher NO�3 -N pro-portion in soil available N has been interpretedas a sign of N saturation (Aber et al., 1998).Furthermore, nitrogen concentrations of plantleaves in mature forest (ranging from 0.95% to2.54%) were higher than those in other forests(including tropical, subtropical and temperateforests) in China (Mo et al., 2000). Our maturesite has been well protected for 400 years andlong-term N accumulation may have alreadyeliminated any N limitation while elevated Ndeposition in the past half century could induceN saturation (36–38 kg ha)1 y)1, Huang et al.,1994; Zhou and Yan, 2001). This is partially sup-ported by the result in control plots of matureforest, where no significant relationship wasfound between decomposition coefficient and thecorresponding initial litter N concentration (Fig-ure 2). Old-growth forest has long been consid-ered to approach ��N saturation�� status with

higher NO�3 -N export compared to young,aggrading forest (Vitousek and Reiners, 1975). Itis reported that micro-organisms must be nitro-gen limited to respond to nitrogen addition byincreased decomposition rate (Eiland et al., 2001;Jensen and Nybroe, 1999; Kuperman, 1999;Mansson and Falkengren-Grerup, 2003). Second,a nutrient imbalance is likely to occur in matureforest. A balance between concentrations of Nand P is important because litter concentrationsof several nutrients are often correlated, anddecomposition requires balanced proportions ofnutrient necessary for microbial growth (Bergand Matzner, 1997; Kuperman, 1999). This isalso supported by our results, that the decompo-sition rate was negatively correlated with the cor-responding initial litter N/P ratio in control plotsof mature forest (Figure 2). In forest ecosystems,prolonged elevated N deposition may eventuallycause N saturation, where the nutrient balance ofthe plant-soil system is disturbed and the capac-ity of the ecosystem to retain added N isexceeded (Aber, 1992). Thus, it is possible that incomparison with that in control plots, N addi-tion may change litter N/P ratio in N treatedplots from enhanced soil N availability, leadingto a shift in decomposer community to a less effi-cient microflora (Fog, 1988). As a result, somenegative response of litter decomposition rate toN addition occurred in mature forest. Third, ahigher N retards the decomposition rate in olderand more humified material in the late stage ofdecomposition. The most negative effect of Naddition on decomposition rate in our study wasfound in the later stage of decomposition(Table 3, Figure 1). During later stages, lignolyt-ic enzyme efficiency maybe limited by high Ncontent or by high available of inorganic N(Berg, 1986; Berg et al., 1998; Fog, 1988; Haged-orn et al., 2003; Magill and Aber, 1998; Mickset al., 2004).

In conclusion, mature forest, which has likelybeen N saturated due to both long-term high Ndeposition in the region and its relatively undis-turbed state of development (no human distur-bance for more than 400 years), had high litterdecomposition rates and exhibited no positiveand some negative effect of nitrogen addition onlitter decomposition. Both disturbed and rehabili-tated forests, which are still N limited due to pre-vious land use history, exhibited lower litter

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decomposition rates that were positively affectedby nitrogen additions. These results suggest thatlitter decomposition and its responses to N addi-tion in subtropical forests of China vary depend-ing on the nitrogen status of the ecosystem. Ourresults were evaluated for just one site of eachforest type, so this study should not be general-ized broadly to all forests in subtropical China.However, these processes and their implicationswould be worth further investigation in otherregions.

Acknowledgments

This study was founded by National Natural Sci-ence Foundation of China (No. 30270283), FieldFrontiers Project of Chinese Academy of Sci-ences Knowledge Innovation Program (KSCX2-SW)133), Director Foundation of South ChinaInstitute of Botany, Chinese Academy of Sci-ences, and the Provincial Natural Science Foun-dation of Guangdong, China (No. 021524). Wethank the two anonymous reviewers for theirvaluable comments and suggestions on the man-uscript.

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Section editor: L.S. Jensen

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