Effects of nitrogen-fixing and non-nitrogen-fixing tree species on soil properties and nitrogen transformation during forest restoration in southern China

ORIGINAL ARTICLE

Effects of nitrogen-fixing and non-nitrogen-fixing tree species onsoil properties and nitrogen transformation during forestrestoration in southern China

Faming WANG1,2, Zhian LI1, Hanping XIA1, Bi ZOU1, Ningyu LI1,2, Jin LIU1,2

and Weixing ZHU3

1Heshan National Field Research Station of Forest Ecosystem, South China Botanical Garden, Chinese Academy of Sciences,

Guangzhou 510650, 2Graduate University of Chinese Academy of Sciences, Beijing 100049, China, and 3Department of Biological

Sciences, State University of New York – Binghamton, Binghamton, New York 13902, USA

Abstract

The role of different plantation tree species in soil nutrient cycling is of great importance for the restoration of

degraded lands. The objective of the present study was to evaluate the potential of N-fixing and non-N-fixing

tree species to recuperate degraded land in southern China. The soil properties and N transformations in six for-

est types (two N-fixing plantations, three non-N-fixing plantations and a secondary shrubland) established in

1984 were compared. The N-fixing forests had 40–50% higher soil organic matter and 20–50% higher total

nitrogen concentration in the 0–5 cm soils than the non-N-fixing forests. Soil inorganic N was highest under the

secondary shrubland. The N-fixing Acacia auriculiformis plantation had the highest soil available P. There were

no significant differences in soil N mineralization and nitrification among the forest types, but seasonal variation

in these N processes was highly significant. In the rainy season, the rates of N mineralization (7.41–11.3 kg N

ha)1 month)1) were similar to values found in regional climax forests, indicating that soil N availability has

been well recovered in these forest types. These results suggest that N-fixing species, particularly Acacia

mangium, are more efficient in re-establishing the C and N cycling processes in degraded land in southern

China. Moreover, the N-fixing species A. auriculiformis performed better than other species in improving soil P

availability.

Key words: afforestation, nitrogen mineralization, nitrogen-fixing species, soil chemical properties, South China.

INTRODUCTION

Subtropical and tropical forests are among the most pro-

ductive terrestrial ecosystems on earth. However, millions

of hectares of subtropical and tropical forests are being

deforested or degraded as a result of human activities

(Lamb et al. 2005). Thus, restoration at both regional and

global scales is critical for the sustainability of the earth’s

ecosystem (Gardiner et al. 2003).

The roles that different tree species (e.g. N-fixing versus

non-N-fixing species, coniferous versus deciduous) play in

restoring soil processes have been extensively studied

(Alvarez-Aquino et al. 2004; Franco and De Faria 1997;

Lamb 1998; Macedo et al. 2008; Malcolm et al. 2008;

Russell et al. 2007). Nitrogen-fixing species, owing to

their ability to fix N2 through microbial symbiosis, can

increase soil C and N and have been widely used as pio-

neer plants in the recovery of degraded land in the tropics

and subtropics (Fisher 1995; Johnson and Curtis 2001).

In Brazil, for example, N-fixing tree species have been suc-

cessful in revegetating degraded land, mostly as a result of

their contribution of 12 Mg ha)1 year)1 dry litter and

0.19 Mg ha)1 year)1 N (Franco and De Faria 1997).

Macedo et al. (2008) also found that using N-fixing spe-

cies (Acacia auriculiformis and Acacia mangium among

others) for the recovery of tropical forests increased soil C

and N stocks by 1.73 and 0.13 Mg ha)1 year)1, respec-

tively. In Australian degraded subtropical land, intention-

ally elevated densities of N-fixing species tended to

increase the litter and soil N content when re-establishing

Correspondence: Z. LI, Heshan National Field Research Stationof Forest Ecosystem, South China Botanical Garden, ChineseAcademy of Sciences, Xingke Road 723, Tianhe District,Guangzhou 510650, China. Email: [email protected]

Received 16 October 2009.Accepted for publication 4 January 2010.

� 2010 Japanese Society of Soil Science and Plant Nutrition

Soil Science and Plant Nutrition (2010) 56, 297–306 doi: 10.1111/j.1747-0765.2010.00454.x

a self-sustaining eucalyptus forest (Grant et al. 2007). In

these studies, both the soil organic matter (SOM) and soil

N content were increased by N-fixing trees.

Nitrogen mineralization, a major process supplying

mineral N to plants in terrestrial ecosystems, is a soil

microbial process that is regulated by many abiotic and

biotic factors (Hayatsu et al. 2008; Matsuoka et al. 2006;

Sano et al. 2006). The use of N-fixing tree species in forest

restoration also greatly affects the rates of N mineraliza-

tion and other N transformations (Knoepp and Swank

1998; Knops et al. 2002). Rhoades et al. (1998) found

that nitrification rates were fivefold faster and NO3 pools

fourfold greater under N-fixing trees than under pasture

grasses. Scowcroft et al. (2004) also reported significantly

increased N availability in surface soils as a result of refor-

estation with koa, an N-fixing tree native to Hawaii. In

Brazil, researchers found that rapid N accumulation by

N-fixing tree species caused higher soil nitrification rates

over immobilization (Siddique et al. 2008).

Southern China, located mostly in a subtropical region,

has 25 million hectares of forest plantations, most of

which have been established on degraded land (Peng et al.

2009; Ren et al. 2007). Nitrogen-fixing Acacia spp. were

introduced to this region in the 1960s as afforestation

trees to conserve water and soil and to improve soil fertil-

ity in degraded areas (Yang et al. 2009). Although the role

of different tree species in restoring soil processes has been

investigated in numerous studies, only a few studies have

been conducted in southern China, and most of these have

focused on the effects of forest management and conver-

sion (Mo et al. 2003; Xiang et al. 2009; Yan et al. 2008).

Specific knowledge on N-fixing species and non-N-fixing

species in forest restoration in this region is still scarce.

In the present study, we investigated soil properties and

N transformations in two N-fixing species plantations,

one eucalyptus plantation, two native species plantations

and one secondary shrub, all of which were established in

1984 on a degraded grassland site. The objective of the

present study was to compare soil properties and N trans-

formations among the six forest types to evaluate the

potential of N-fixing and non-N-fixing species to recuper-

ate degraded land in southern China.

MATERIALS AND METHODS

Study area

The experimental site is located at the Heshan National

Field Research Station of Forest Ecosystems (60.7 m

a.s.l., 22�34¢N, 112�50¢E), which is in the subtropical

region of southern China (Fig. 1). The region has a sub-

tropical monsoon climate. The mean annual temperature

is 21.7�C, the mean annual rainfall is 1,700 mm and the

annual potential evaporation is approximately 1,600 mm

(Fig. 2). The annual cycle includes a hot and rainy (grow-

ing) season (from April to September) and a cool and dry

(dormant) season (from October to March). Climax vege-

tation in this region is subtropical evergreen broad-leaved

forest. As a result of long-term disturbances, the soil in

this area has eroded and the original vegetation has almost

disappeared, leading to vast areas of degraded land (Yu

and Peng 1996).

Experimental design

The experimental area is typical of the region, with low

hills (<30 m vertical distance between the lowest and

highest points) and small catchments (each having an area

of approximately 5–8 ha). The slope of the area is

between 20 and 30� and the soil type is classified as an

acrisol developed from sandstone, with a pH of approxi-

mately 4.0. In 1984, six adjacent catchments vegetated

only with grass were chosen for a scientific study on the

basis of their similarity. Five experimental plantations

(Eucalyptus citriodora monoculture, Acacia mangium

monoculture [N-fixing], Acacia auriculiformis monocul-

ture [N-fixing], Schima superba monoculture and a native

species mixed plantation [mainly Schima wallichii and

Castanopsis hystrix]) were randomly allocated to each

catchment and trees were planted on a 2.5 m · 3 m grid.

There was also an unplanted area (approximately 2 ha)

Figure 1 Map of study site (Heshan station).

Figure 2 Monthly mean soil temperature (measured at a soildepth of 5 cm) and rainfall amount at Heshan station in 2007.


298 F. Wang et al.

left to observe the effects of natural revegetation. These

forests have been protected for scientific research since

their establishment (Li et al. 2001). Unfortunately this

design has inherent limitations because site and forest-type

effects are confounded. However, in this particular situa-

tion, the initial soil properties were similar among the

plantations, for example, in 1986, 2 years after

initial planting, the SOM (0–15 cm) ranged from 14.33 ±

1.08 g kg)1 in the eucalyptus plantation to 16.39 ±

0.21 g kg)1 in the A. mangium plantation; this difference

was not significant (Tan 2008). Thus, any differences

found later among plantations can be considered to result

mainly from the forest type because of the homogenous

nature of the experimental area prior to afforestation

(Li et al. 2001). In 2007, three 20 m · 20 m replicate

plots were randomly selected in each forest type (including

the secondary shrubland). Detailed vegetation informa-

tion of the six forest types in 2007 is shown in Table 1.

Soil sampling and measurement of nitrogentransformations

In 2007, an in situ soil-core technique (Raison et al. 1987)

was used to estimate soil net N mineralization and N

leaching rates. Nine sample points were randomly located

in each 20 m · 20 m replicate plot. At each of these

points, two polyvinyl chloride tubes (4.6 cm in diameter

and 15 cm in height) were hammered into the soil to a

depth of 10 cm. Forest floor litter was removed before

sampling. One of the two tubes from each subplot was

retrieved and sent to the laboratory (S0). The other tube,

with a lid on the top and holes on the upper 5 cm sidewall

for aeration, was incubated in situ for 1 month (30 days)

before being retrieved (S1). Initial soil sampling was done

in June and December, representing the typical rainy and

dry seasons in this region.

All soil cores were transported to the laboratory imme-

diately, stored at 4�C and extracted for mineral N within

48 h of sampling. Before extraction, each of the nine cores

from the same plot was manually divided into two layers

(0–5 cm and 5–10 cm) and soils from the same section

(from the same plot) were pooled and mixed thoroughly.

Visible roots and stones were removed manually. Twenty

grams of fresh soil from each layer was extracted with

100 mL of 2 mol L–1 KCl solution (1:5) and filtered

(202# filter paper, Shuangquan Corp., Shanghai, China).

The concentrations of ammonium and nitrate in the

extraction solution were determined using a flow injection

autoanalyzer (FIA) (Lachat Instruments, Loveland, CO,

USA); ammonium was determined using the salicy-

late–nitroprusside method and nitrate by sulfanilamide

colorimetry after the Cd-core reduction to nitrite. Soil

moisture was determined by weight loss after oven-drying

at 105�C for 24 h. Bulk density was calculated based on

the weight of the dried soils in all tubes.

Net N mineralization was calculated as the increase in

ammonium plus nitrate N between the initial soil sample

(S0) and the incubated sample (S1), and net nitrification

was the increase in nitrate. Soil net N mineralization and

nitrification in the 0–10 cm soils were computed as the

summation of changes in the 0–5 cm soil layer and the

5–10 cm layer. Although the method used here may con-

tain some ‘‘artificial’’ effects (e.g. root severing and the

exclusion of a root effect on soil moisture) on soil N pro-

cesses (Jussy et al. 2004), other studies have suggested

that such effects are minor and a short incubation period

(<4 weeks) was recommended to overcome this problem

(Adams et al. 1989; Stenger et al. 1996). In this case, we

incubated for 1 month (30 days), a time period practiced

by many researchers (Uri et al. 2008; Yan et al. 2008).

Soil chemical properties

Soil chemical properties (i.e. soil pH, soil exchangeable

cations, organic matter, total N and C ⁄ N) were deter-

mined using soil samples from the S0 cores collected in

June 2007. All soil samples were air-dried and passed

through a 2 mm sieve. Soil pH was measured in a 1:5

mixture of soil : deionized water. Soil exchangeable K+,

Na+, Ca2+ and Mg2+ were extracted with 1 mol L–1

NH4Ac (Liu et al. 1996) and measured by inductively

coupled plasma (ICP) (Perkin Elmer, Waltham, MA,

USA). Soil available P was extracted with Bray-2 solution

(Bray and Kurtz 1945) and determined using the molyb-

date blue colorimetric method. Soils for the analyses of

total N (TN) and organic matter were ground to pass

through a 0.25-mm sieve. The TN concentration was

determined by micro-Kjeldahl digestion followed by col-

orimetric determination on the Lachat FIA. Soil organic

carbon (SOC) was determined using the wet combustion

method, and SOM was calculated as SOM = 1.73 · SOC

(Liu et al. 1996). The soil C ⁄ N ratio was calculated as the

ratio of SOC to soil TN.

Table 1 Vegetation description of the six forest types (includinga shrubland) at Heshan Station

Forest type Main species

Height

(m)

Coverage

(%)

d.b.h.

(cm)

AM Acacia mangium 20.3 90 23.2

AA Acacia auriculiformis 19.4 80 22.5

EU Eucalyptus citriodora 25.4 90 18.5

SS Schima superba 12.1 80 14.3

MX Schima wallichii 12.3 80 13.6

Castanopsis hystrix 11.2 12.7

SL Litsea cubeba 3.3 60 –

Evodia lepta 5.6 –

Data were collected in October 2007, 23 years after the initial planting.AA, Acacia auriculiformis; AM, Acacia mangium; d.b.h., diameter atbreast height; EU, Eucalyptus citriodora; MX, native species mixture;SL, secondary shrubland; SS, Schima superba.


Nitrogen-fixing species in forest restoration 299

Statistical analyses

In the present study, all soil variables in the six forest types

were measured in 0–5 cm soils and 5–10 cm soils sepa-

rately. A two-way ANOVA, with forest type (including sec-

ondary shrubland, n = 6) and soil depth (n = 2) as the

main factors, was used to analyze the respective effects of

forest type and soil depth (as well as their interactions) on

soil NH4+, NO3

), available P and other soil properties

(SOM, TN, C ⁄ N, bulk density, soil pH and exchangeable

cations). In each soil layer, if a significant effect of forest

type was found, a least significant difference post-hoc test

was carried out after a one-way ANOVA to test the differ-

ences of the above variables between the two specific forest

types. Area-based (0–10 cm soils) measurements of N

transformations in each season, including N mineralization

rates and nitrification rates, were analyzed using a one-way

ANOVA. The equality of variance in the data was tested by

Levene’s test. As the variances of exchangeable K+, Na+,

Ca2+ and Mg2+ were not homogeneous, a non-parametric

rank analysis (Scheirer–Ray–Hare test) was used for these

variables (Scheirer et al. 1976). Pearson correlation was

used to detect any relationships among soil pH, SOM, TN

and exchangeable K, Na, Ca and Mg. All analyses and

computations were carried out in SPSS 15.0 (SPSS Inc.,

Chicago, IL, USA) and Excel 2003 (Microsoft Corp., Red-

mond, WA, USA) software.

RESULTS

Soil carbon and nitrogen pools and pH

Soil organic matter and TN concentration all varied sig-

nificantly among forest types and between soil depths

(Table 2). There was also a significant positive correlation

between SOM and TN (P < 0.01; Table 3). In the 0–5 cm

soils, plantations of the N-fixing species A. mangium and

A. auriculiformis had significantly higher SOM and TN

concentrations than the E. citriodora, S. superba and

mixed native species plantations (Table 2). In the 5–

10 cm soils, however, there was no difference among the

forest types (Table 2). Both SOM and TN concentrations

decreased with soil depth. Soil C ⁄ N ratios did not differ

among forest types (Table 2), but were significantly higher

in the 0–5 cm soils than in the 5–10 cm soils (P < 0.001).

Soil pH was similar among the six forest types

(Table 2). For example, in the 0–5 cm soil, the highest pH

value (3.88) was found in the mixed plantation and in the

Eucalyptus plantation, but this value was only 0.07 pH

unit higher than the lowest value (3.81), which was

recorded in the A. mangium plantation. The pH in the 0–

5 cm soils was significantly lower than that in the 5–

10 cm soils (P < 0.05), in accordance with higher SOM

concentration in the 0–5 cm soils. In the correlation anal-

ysis, soil pH was mainly negatively related to SOM and

TN (P < 0.05; Table 3).

Soil exchangeable cations

Soil exchangeable cations varied significantly among for-

est types, with the exception of Mg2+, which varied

greatly among replicates and had no pronounced varia-

Table 2 General soil properties in the 0–5 cm and 5–10 cm soils of the six forest types at Heshan station in 2007

Variables Soil layer AM AA EU SS MX SL Ft Sd Ft · Sd

SOM (g kg)1) 0–5 cm 78.9c ± 3.78 73.4b ± 7.68 50.2a ± 4.42 49.4a ± 6.55 46.3a ± 9.89 52.0ab ± 2.69 <0.01 <0.001 ns

5–10 cm 32.6 ± 4.03 28.5 ± 4.55 30.2 ± 9.17 23.5 ± 3.80 17.6 ± 3.28 29.1 ± 2.17

TN (g kg)1) 0–5 cm 1.39c ± 0.08 1.13b ± 0.10 0.91a ± 0.01 0.84a ± 0.01 0.88a ± 0.07 0.98ab ± 0.05 <0.01 <0.001 <0.01

5–10 cm 0.68 ± 0.03 0.71 ± 0.07 0.73 ± 0.11 0.64 ± 0.10 0.73 ± 0.06 0.66 ± 0.05

C ⁄ N 0–5 cm 33.2 ± 2.33 37.4 ± 4.97 32.1 ± 2.72 33.8 ± 4.27 30.5 ± 4.26 30.7 ± 0.09 ns <0.001 ns

5–10 cm 27.7 ± 2.38 23.1 ± 2.02 26.5 ± 10.3 21.4 ± 5.05 15.4 ± 1.71 26.0 ± 2.00

BD (g cm)3) 0–5 cm 0.88 ± 0.03 1.04 ± 0.07 0.91 ± 0.04 1.01 ± 0.03 0.98 ± 0.07 0.99 ± 0.05 <0.05 <0.001 ns

5–10 cm 1.16ab ± 0.02 1.31c ± 0.02 1.27bc ± 0.02 1.17abc ± 0.06 1.04a ± 0.09 1.25bc ± 0.04

Soil pH 0–5 cm 3.81 ± 0.02 3.85 ± 0.03 3.88 ± 0.04 3.87 ± 0.04 3.88 ± 0.03 3.85 ± 0.02 <0.05 <0.05 ns

5–10 cm 3.81 ± 0.06 3.92 ± 0.02 3.94 ± 0.02 3.96 ± 0.04 3.97 ± 0.03 3.85 ± 0.03

AA, Acacia auriculiformis; AM, Acacia mangium; BD, bulk density; EU, Eucalyptus citriodora; Ft, forest types effects; MX, native species mixture; Sd, soildepth effects; SL, secondary shrubland; SOM, soil organic matter; SS, Schima superba; TN, total nitrogen. Data are mean ± standard error (n = 3). In eachlayer, a one-way ANOVA was used to detect differences among forest types; means sharing the same superscript were not significantly different at P = 0.05(least significant difference).

Table 3 Pearson’s correlation analysis of soil pH, soil organicmatter, total nitrogen and exchangeable K, Na, Ca and Mg

pH K Na Ca Mg SOM

K )0.016 1

Na )0.046 )0.166 1

Ca )0.107 )0.324 0.550* 1

Mg )0.535* 0.005 0.267 0.478* 1

SOM )0.720** 0.050 0.507* 0.199 0.660**

TN )0.511* )0.097 0.567* 0.447 0.674** 0.732**

Significant correlations are indicated as follows: *P < 0.05, **P < 0.01.Sample sizes are 18 for all variables. This analysis was based on the aver-age values of these variables in the 0–5 cm and 5–10 cm soils. SOM, soilorganic matter; TN, total nitrogen.


300 F. Wang et al.

tion among treatments (Fig. 3). The soil exchangeable K+

concentration under the S. superba plantation was the

highest in both soil layers, and significantly greater than

the values recorded in the other plantations (Fig. 3a,b).

The three exotic-species plantations (E. citriodora,

A. mangium and A. auriculiformis) had approximately

20% higher exchangeable Na+ concentration than the

S. superba plantation and the shrubland in both soil layers

(Fig. 3c,d). For Ca2+, the secondary shrubland had the

lowest concentration among the six forest types in the

0–5 cm and 5–10 cm soils. In particular, almost no

exchangeable Ca2+ was detected in the 5–10 cm soil of

the secondary shrubland.

Soil exchangeable cation concentrations all declined sig-

nificantly with an increase in soil depth (Fig. 3). Soil

exchangeable K+ and Na+ in the 5–10 cm soils were over

70% of those in the corresponding upper soils, whereas

they were only 50% and even less for exchangeable Ca2+

and Mg2+.

Soil inorganic nitrogen and available phosphorus

Soil extractable ammonium varied significantly among the

forest types in both the rainy and dry seasons (Fig. 4a,b;

P < 0.05 for both). In June, the N-fixing A. mangium plan-

tation and the shrubland had the highest soil ammonium

concentration, and ammonium concentrations were

2–6 mg kg)1 lower in the 5–10 cm soil than in the 0–5 cm

soil. The highest ammonium concentration in the 5–10 cm

soil was found under shrubland (8.0 mg kg)1). In Decem-

ber, the shrubland and the A. mangium plantation still had

the highest concentration of ammonium, and the pattern

among forests was similar to that in the rainy season

(Fig. 4b).

Unlike soil ammonium, soil nitrate concentration dif-

fered significantly among forest types, but only in the

rainy season (P = 0.001; Fig. 4c). In June, soil nitrate was

highest under shrubland, followed by the N-fixing

A. mangium in both soil layers (Fig. 4c). In December,

soil nitrate did not differ significantly among forests

owing to large variance within treatments (Fig. 4d).

Soil available P varied significantly among forest types

in the rainy season, but not in the dry season (Fig. 4c,d).

In June, the N-fixing A. auriculiformis plantation had the

highest available P concentration in both soil layers, and

the concentration was significantly higher than that under

Eucalyptus citriodora, A. mangium and the shrubland

(Fig. 4e). In December, the available P concentration

greatly declined, and was only approximately 1.0 mg

kg)1 in both soil layers (Fig. 4f).

Nitrogen mineralization and nitrification

Differences in soil N mineralization and nitrification

among forest types were not significant in either season

(Table. 4). Net N mineralization rates were high in the

rainy season, ranging from 7.4 to 11.3 kg N ha)1

month)1, but negligible or even negative (net immobiliza-

tion) in the dry season. Nitrification dominated the

(a)

(b)

(c)

(d)

Figure 3 Soil exchangeable (a) K+, (b) Na+, (c) Ca2+ and (d)Mg2+ in the 0–5 cm and 5–10 cm soils under the six forest typesat Heshan station (mean ± standard error, n = 3). AA, Acaciaauriculiformis; AM, Acacia mangium; EU, Eucalyptus citriodora;MX, native species mixture; SL, secondary shrubland; SS, Schimasuperba. Bars sharing the same superscript letter are not signifi-cantly different at P = 0.05 (least significant difference).



process of N mineralization. In the rainy season, nearly

100% of mineralized N was nitrified. Soil nitrification

rates were much lower in the dry season than in the rainy

season, which was similar to the trend for N mineraliza-

tion (Table. 4).

DISCUSSION

Effects on soil properties

In the restoration of degraded areas, C input and an

increase in soil N content are of great importance because

they can enhance the capacity of the system to support a

more complex community (Franco and De Faria 1997;

Macedo et al. 2008). Nitrogen-fixing species have been

used as an N source in the recovering of tropical and sub-

tropical systems, including degraded mining land (Franco

and De Faria 1997), deforested land (Siddique et al.

2008) and agroforestry (Handayanto et al. 1995). In these

studies, not only soil N, but also SOM has been increased

by N-fixing species (Deans et al. 1999; Franco and De

Faria 1997; Macedo et al. 2008). The SOM and TN

results in the present study also showed that the two

N-fixing species (A. mangium and A. auriculiformis) were

able to restore C and N cycling better than the non-N-fix-

ing species and natural revegetation (shrubland) in south-

ern China; these results are consistent with observations

from other tropical and subtropical regions (Macedo et al.

2008; Siddique et al. 2008; Stock et al. 1995).

The higher SOM and TN concentration in the 0–5 cm

soils, relative to the non-N-fixing plantations (Table 2),

may result from higher litter production and lower litter

decomposition of N-fixing species. It is known that litter

production and the rate of litter decomposition are the

most important factors by which tree species regulate the

(a) (b)

(c) (d)

(e) (f)

Figure 4 (a, b) Soil extractable ammonium, (c, d) nitrate and (e, f) available P in the rainy season (a,c,e) and (b,d,f) dry season of 2007in the six forest types at Heshan station (mean ± standard error, n = 3). AA, Acacia auriculiformis; AM, Acacia mangium; EU, Eucalyp-tus citriodora; MX, native species mixture; SL, secondary shrubland; SS, Schima superba. Bars sharing the same superscript letter are notsignificantly different at P = 0.05 (least significant difference).


302 F. Wang et al.

size and distribution of soil C and N pools (Aerts and de

Caluwe 1997; Finzi et al. 1998a; Stump and Binkley

1993). Li et al. (2000) reported litter-fall mass at this site

in the order of A. mangium (11.1 t ha)1) > S. superba

(6.5 t ha)1) > A. auriculiformis (4.8 t ha)1) > Eucalyptus

citriodora (2.6 t ha)1). In addition, the litter of N-fixing

A. mangium and A. auriculiformis had a much lower

decomposition rate compared with other species (Euca-

lyptus citriodora and S. superba) (Li et al. 2000, 2001).

Thus, the large differences in litter production and the rate

of litter decomposition between N-fixing and non-N-fix-

ing species may have contributed to the higher soil C and

N pools under the two N-fixing species.

In the present study, an acidification effect by N-fixing

tree species was not significant. However, previous studies

have shown that N-fixing species acidified their rooting soil

more than non-N-fixing species (Haynes 1983). For exam-

ple, in Hawaii, Rhoades and Binkley (1996) observed that

soil pH declined more dramatically (from 5.9 to 4.5) in an

N-fixing (Albizia) plantation than in a Eucalyptus planta-

tion (from 5.9 to 5.0). Yamashita et al. (2008) also found

that the surface soil pH in an 8-year-old N-fixing A. man-

gium plantations was 1 pH unit lower than that in a non-

N-fixing Imperata cylindrica grassland. In the present

study, however, there was very little difference (0.1 unit)

in soil pH between the N-fixing and non-N-fixing species

in either the 0–5 cm or the 5–10 cm soils (Table 2).

Although nitrogen fixation and nitrification processes

could lead to soil acidification, other factors, such as initial

soil condition, atmospheric acid deposition, the export of

cations by leaching or plant uptake and litter decomposi-

tion, could also acidify soil (Finzi et al. 1998b; Yamashita

et al. 2008). At the present site, soil pH in the initial soil

condition was strongly acidic, below pH 4.2 (Yu and Peng

1995). As soil has a strong buffering capacity in acidic con-

ditions owing to dissolving aluminum from clay minerals

(van Breemen et al. 1984), these buffering processes may

contribute to the insignificant difference between the

N-fixing and non-N-fixing sites. Another possibility is that

there is no significant difference in nitrification rates

among forest types. Nitrification could reduce soil pH by

producing protons in its chemical processes, thus resulting

in a decline in soil pH under N-fixing tree sites.

The soil in the N-fixing A. auriculiformis plantation

had the highest available P concentration in both soil lay-

ers. We also observed a higher soil available P concentra-

tion under A. auriculiformis seedlings than under other

species, such as A. mangium and S. superba, in a pot

experiment (Wang F, 2009, unpubl. data). In southern

China, P deficiency is a general problem for most planta-

tions (Ren et al. 2007). Thus, Acacia auriculiformis may

be a better choice to improve soil P availability in com-

parison to other species. As tree species can regulate soil

P availability through their effect on soil pH and phos-

phatase activities (Zou et al. 1995), further studies

should be done to show that A. auriculiformis can affect

soil P availability.

Effects on soil nitrogen transformations

There were no significant differences in N mineralization

or nitrification between the N-fixing species and the non-

N-fixing species in the present study. This result differed

from previous studies, which have demonstrated that soils

under N-fixing species had higher N transformation rates

than those under non-N-fixing species (Bernhard-Reversat

1988; Siddique et al. 2008). Our result was also inconsis-

tent with observations made in these plantations after

13 years of growth, when Li et al. (2001) found that nitri-

fication rates in the two N-fixing species plantations were

much greater than those in the non-N-fixing E. citriodora

and S. superba stands. One possibility is that over

20 years other sources of N input, such as regional atmo-

spheric deposition, have greatly increased N availability in

all forests. Fang et al. (2008) measured high inorganic N

deposition in this region at a rate of over 30 kg N ha)1

year)1 and another 10–20 kg N ha)1 year)1 deposition in

the form of dissolved organic N.

In the present study, net N mineralization rates in the

rainy season ranged from 7.41 to 11.3 kg N ha)1

month)1 (Table 4). The rates in these forests are similar to

values found in climax forest in this region. In the Dinghu-

shan climax evergreen broad-leaved forest, 65 km from

our sites, Fang (2006) detected a 6.7 kg N ha)1 month)1

soil N mineralization rate. Li et al. (2006) worked in an

evergreen broad-leaved forest in Yunnan Province and

found that annual N mineralization in the 0–15 cm soils

was 159.12 kg N ha)1 year)1, equivalent to 12–18 kg N

ha)1 month)1. We estimated that the annual N minerali-

zation rate of the 0–10 cm soils in the six forest types

ranged from 60 to 100 kg N ha)1 year)1. Thus, the val-

Table 4 Net nitrogen mineralization and nitrification rates (datawere combined in the 0–10 cm soils) in the six forest types atHeshan station in 2007

Forest

type

Nitrogen mineralization

(kg N ha)1 month)1)

Nitrification (kg N ha)1

month)1)

Rainy Dry Rainy Dry

AM 11.0 ± 1.62 )1.46 ± 1.93 14.51 ± 1.85 0.37 ± 0.54

AA 10.9 ± 2.08 0.93 ± 0.92 14.67 ± 1.40 4.09 ± 0.35

EU 8.56 ± 3.24 )2.46 ± 0.86 11.04 ± 2.95 1.27 ± 0.94

SS 11.3 ± 2.96 )2.01 ± 0.81 14.25 ± 2.24 1.44 ± 1.62

MX 7.41 ± 1.09 )0.78 ± 0.90 10.36 ± 1.12 1.79 ± 0.2

SL 8.03 ± 1.99 1.68 ± 3.14 10.30 ± 2.10 1.82 ± 0.41

P-value ns ns ns ns

AA, Acacia auriculiformis; AM, Acacia mangium; EU, Eucalyptus citrio-dora; MX, native species mixture; SL, secondary shrubland; SS, Schimasuperba. Data are mean ± standard error (n = 3).



ues were similar to those found in natural climax forests

of subtropical China. Based on the study in Dinghushan,

Mo et al. (2003) suggested that over a period of approxi-

mately 50 years, successful rehabilitation of soil N avail-

ability on severely degraded lands is possible. However,

our results suggested that soil N availability could be

mostly recovered after 23 years of forest restoration.

Contrary to our expectations, soil inorganic N, particu-

larly nitrate, was highest not under the two N-fixing plan-

tations, but under the naturally regenerated shrubland.

This result differs from the patterns of soil total N pools

(Table. 2). In general, variations in soil inorganic N can

be attributed to three factors: plant uptake, N mineraliza-

tion and nitrification, and losses through leaching. As

there were no differences in soil N mineralization and N

leaching loss (data not shown) among forest types in the

present study, plant uptake is probably the main factor

that led to the variation in soil inorganic N. In a 2007 sur-

vey, the height of the overstory vegetation was less than

6 m in the shrubland and over 10 m in the plantations

(Table 1). In the A. mangium and E. citriodora stands,

the tallest trees were over 25 m. Therefore, it is likely that

the low plant uptake in the shrubland explains the high

inorganic N concentration in that system.

Conclusions

Soil properties and N transformations in six forest types

were compared in the present study to evaluate the effects

of N-fixing and non-N-fixing species on forest restoration

in southern China. The N-fixing forests had 40–50%

higher SOM and 20–50% higher TN concentration in the

0–5 cm soils than the non-N-fixing forests, suggesting that

N-fixing species, particularly A. mangium, are more effi-

cient in re-establishing C and N cycling processes in the

degraded land of southern China. There were no signifi-

cant differences in soil N mineralization and nitrification

among the forest types. In the rainy season, the rates of N

mineralization (7.41–11.3 kg N ha)1 month)1) were sim-

ilar to values in regional climax forests, indicating that soil

N transformations have been well recovered in these 23-

year-old plantations. Soil inorganic N was highest under

the secondary shrubland and second highest under the

N-fixing Acacia mangium. Lower plant uptake could be

responsible for the higher inorganic N in the shrubland.

The present results show that after 23 years’ growth,

N-fixing species performed better in restoring soil C and

N pools and their cycling.

ACKNOWLEDGMENTS

The project was supported by National Basic Research

Program of China (973 Program, 2009CB421101) and

the National Natural Science Foundation of China

(30630015 and 30870442). We also thank Professor

Murray McBride from Cornell University and Dylan Hor-

vath and Tim Scott from Binghamton University-SUNY

for their critical comments on this manuscript.

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Effects of nitrogen-fixing and non-nitrogen-fixing tree species on soil properties and nitrogen transformation during forest restoration in southern China