Acta Ecologica Sinica 35 (2015) 3543

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Acta Ecologica Sinica

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / c h n a e s

Impacts of nitrogen deposition on soil nitrogen cycle in forest

ecosystems: A review
Xiaomin Zhu a,b, Wei Zhang a, Hao Chen a,b, Jiangming Mo a,*
a Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences,

Guangzhou, Guangdong 510650, China

b University of Chinese Academy of Sciences, Beijing 100049, China

A R T I C L E I N F O A B S T R A C T

Article history: Atmospheric nitrogen (N) deposition has accelerated in the last several decades due to anthropogenic
Received 16 October 2013 activities, such as nitrogen fertilization, N-xing plants cultivation and fossil fuel and biomass combus-
Revised 28 March 2014 tion. Increasing N deposition has become one of the important factors regulating N cycle in forest
Accepted 7 May 2014
ecosystems. Forest ecosystems can retain part of deposited N in soil by biotic and abiotic mechanisms,
Available online
but when N inputs exceed the capacity of soil retention, N losses will aggravate in terms of N oxide emis-
sion and/or nitrate leaching. The excess N input has threatened ecosystem health via acidication and
Keywords:
eutrophication, causing declines in terrestrial biodiversity and forest productivity in forest ecosystems
N deposition
Soil nitrogen cycle of Europe and North America. Recently, China has become one of the three areas that undergo severe N
Forest ecosystems deposition in the world. Impacts of N deposition on soil N cycle in Chinese forest ecosystems have re-
ceived increasing concern. In this paper, we reviewed the processes of soil N cycle and their responses
to atmospheric N deposition based on available literature. The objective is to enhance our understand-
ing on how N deposition affects soil N cycle in forest ecosystems and provide scientic information for
sustainable forest management. The review mainly includes the following four aspects: (1) processes of
soil N cycle and their controlling factors. These processes include biological N xation (BNF), decompo-
sition, mineralization, nitrication, denitrication, N oxide emission and NO3N leaching. The controlling
factors of these processes are complicated and interactional. Only one of these factors altered may affect
soil N cycle. For example, C/N is the factor that controls BNF, decomposition, mineralization and NO3N
leaching. (2) Research methods and current results about studies are related to the impact of N depo-
sition on soil N cycle in forest ecosystems. In general, the research methods are long-term simulated N
deposition experiment, N deposition gradient method, roof clean rain method and 15N tracing method.
Effects of N deposition on soil N cycle vary depending on different initial N statuses and lengths of ex-
periment. In N-limited forests, N deposition tended to have positive effect on soil N cycling processes,
such as accelerating litter decomposition rate and N mineralization rate. However, such result generally
showed in short-term fertilization experiments. In some long-term fertilization experiments, it
showed that the negative effects would rise when the forests reached N saturation. Compared to
N-limited forests in temperate region, N deposition tended to have negative or neutral effects in
N-rich tropical forest. For example, N deposition promoted nitrication process in tropical forests.
(3) Possible mechanisms for the effect of N deposition on soil N cycle: N deposition can affect soil N cycle
through altering the chemical characteristic of forest substrates, the biomass and community composi-
tion of plant and microorganism. (4) Current problems and future research needs for the study about
the effect of N deposition on soil N cycle: What role does regional diversity, changes in forest type, and
interaction of carbon (C), N and phosphorus (P) play on the effect of N deposition on soil N cycle in forest
ecosystems deserve our further study in the future.
2015 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

* Corresponding author. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences,
Guangzhou, Guangdong 510650, China. Tel.: +86-758-2621187; fax: +86-758-2623242.
E-mail address: mojm@scib.ac.cn (J. Mo).

http://dx.doi.org/10.1016/j.chnaes.2015.04.004
1872-2032/ 2015 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
36 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543

Contents

1. Processes of soil N cycle .................................................................................................................................................................................................................................... 36

1.1. N input ....................................................................................................................................................................................................................................................... 37
1.2. Soil N transformation ........................................................................................................................................................................................................................... 37
1.3. Soil N output ............................................................................................................................................................................................................................................ 37
2. Study methods for the effect of N deposition on soil N cycle in forests .......................................................................................................................................... 38
3. The effect of N deposition on soil N cycle in forests ............................................................................................................................................................................... 38
3.1. The effect of N deposition on soil N input .................................................................................................................................................................................... 38
3.1.1. Effects of N deposition on BNF ......................................................................................................................................................................................... 38
3.1.2. Effects of N deposition on litter decomposition and nutrient dynamic ............................................................................................................. 38
3.2. The effect of N deposition on soil N transformation ................................................................................................................................................................. 40
3.3. The effect of N deposition on soil N output ................................................................................................................................................................................. 40
4. Mechanisms for N deposition effects on soil N cycling .......................................................................................................................................................................... 40
4.1. Altered litter and forest substrates chemical qualities ............................................................................................................................................................. 40
4.2. Altered plant biomass and the structure of communities ...................................................................................................................................................... 41
4.3. Changed the activity and composition of microbial communities ...................................................................................................................................... 41
5. Problems and prospects .................................................................................................................................................................................................................................... 41
5.1. Differences between regions .............................................................................................................................................................................................................. 41
5.2. Changes of forest type ......................................................................................................................................................................................................................... 41
5.3. Limitations of study .............................................................................................................................................................................................................................. 41
5.4. Relationships between C, N and P ................................................................................................................................................................................................... 42
Acknowledgements ............................................................................................................................................................................................................................................. 42
References .............................................................................................................................................................................................................................................................. 42

Soil N pool occupies for nearly 90% of total N storage in forest enhanced our understandings of the effect of N deposition on struc-
ecosystem. Soil N cycle is an essential component to determine the ture and function of tropical forest ecosystems [1722]. In-situ soil
rate of ecosystem N cycle and euxes [1,2]. Soil N cycle in forest core incubation, ion exchange resin and 15N isotopes tracer tech-
ecosystems constitutes three processes, such as input, transforma- nique were used to examine the size of soil N pool and soil uxes
tion and output. These processes include: biological N xation (BNF), in these studies.
litter decomposition, N mineralization, nitrication, denitrica- Recently, China has become one of the three areas that undergo
tion, N-oxide emission and N leaching [1]. With less or no human severe N deposition in the world [4]. In China, average rate of N
disturbance, soil N in forest ecosystem mainly comes from BNF and deposition increased from 13.2 kg N hm 2 year 1 in 1960s to
decomposition. N element transfers among plant, microorganism, 21.1 kg N hm2 year1 in 2000s [22]. N deposition rates have reached
soil organic matter and soil mineral matter, while less N loss occurs 3050 kg N hm2 year1 in Southeast China, and these rates were
in these ecosystems [2,3]. However, N deposition has elevated in higher than the peak value of N deposition in Europe and the United
the past several decades, due to N fertilization, N-xing plants cul- State. It means that large amount of N will transport into the forests
tivation, and fossil fuel and biomass combustion [4]. Galloway et al. by deposition [2,23]. However, no attention was paid to assess the
[4,5] forecasted global N deposition would reach 200 Tg N year1 in effect of N deposition on forest ecosystem in China until the rst
2050 and it has become the main pattern of N input in forests. Forest study site was established in Dinghushan Biosphere Reserve (DHSBR)
ecosystems can retain part of deposited N in soil by biotic and abiotic in southern China in 2003 [9]. After that, study sites were con-
mechanisms, such as plant uptake, microbial immobilization, soil ducted in other subtropical areas (Fujian, Chongqing, Sichuan, etc.)
cation exchange capacity and soil organic matter absorption [6,7]. and temperate areas (Changbaishan mountain) in China [23].
But when forest ecosystems reach N saturation, plant and micro- However, our understanding of the responses of soil N cycle and
organism cannot accumulate excess N any more [8]. At this point, N transformation to N deposition in forest ecosystems was still
N will loss from ecosystem by leaching and N-oxide emissions, re- limited. There were two reviews to summarize the effect of N de-
sulting in water pollution and increasing greenhouse gas emissions position on ecosystem: the former only focused on the processes
[9,10]. According to many studies in temperate and tropical forests, of soil N transformation (mineralization, nitrication and denitri-
excess N input has altered structure and function of forest ecosys- cation) [2]; the latter focused on the different effects of N deposition
tems. For examples, N deposition may inhibit plant growth by on N pools and N cycling between agriculture ecosystem and non-
breaking the balance of elements, reduce biological diversity by soil agriculture ecosystem, without mentioning the related mechanisms
acidication, and cause forest degeneration in the most serious sit- [24]. In this paper, we reviewed the processes of soil N cycle and
uation [11,12]. The ecological and environmental issues aroused by their responses to atmospheric N deposition in temperate and trop-
N deposition have received increasing concern. ical forests based on available literatures. We also discussed the
The effect of N deposition on forest ecosystem has been studied possible mechanisms for the effect of N deposition on soil N cycle.
in temperate zone early in 1980s, for examples, nitrogen satura- The objective is to enhance our understanding on how N deposi-
tion experiments (NITREX) and experimental manipulation of forest tion affects soil N cycle in forest ecosystems and to provide scientic
ecosystems (EXMAN) programs in Europe [13,14]. In the U.S., study information for sustainable forest management.
sites were established later in Harvard forest in Massachusetts, the
Bear Brook watershed in Maine, and Mt. Ascutney forest in Vermont
[15,16]. These studies proposed the response of N-limited forests 1. Processes of soil N cycle
to N deposition and the related mechanisms. As N deposition has
elevated in tropical zones, the effect of N deposition on tropical forest Soil N cycle is one key components of N cycle in forest ecosys-
ecosystems has received wide concerns. Currently, long-term study tems. It is also the most important and active processes in ecosystem
sites were established in many tropical zones, such as Hawaii, Costa N cycle [1,2]. Soil N cycle in forest ecosystem constitutes three pro-
Rice, Puerto Rico, Ecuador, and Panama. The ndings from these sites cesses, such as input, transformation and output. These processes
 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543
Plant biomass N pool
Biological
nitrogen fixation1 Nitrogenase
Litter or organic
decomposition2
Ammonification3
NH3 volatilization6
Fig. 1. Nitrogen pools and key processes of nitrogen cycle in forest ecosystems. N input: 1, 2; N transformation: 35; N output: 68.
include: BNF, litter decomposition, N mineralization, nitrication,
denitrication, N oxide emission and leaching [1,2,7] (Fig. 1).
1.1. N input
BNF is a process that N-xing microorganisms convert atmo-
spheric dinitrogen (N2) to ammonia by nitrogenases [25]. In the
absence of human activities, biotic N xation is the primary source
of reactive N, providing about 90130 Tg N year1 on the conti-
nents [26]. According to the relationship between diazotrophs and
other organisms, N-xers can be divided into three types: symbi-
otic N-xers (rhizobia), nonsymbiotic N-xers (free-living N-xers,
cyanobacteria) and lamentous actinomycetes (x nitrogen as free-
living microorganisms or in symbiosis with a number of non-
leguminous vascular species) [27]. In general, the diazotrophs which
symbioses with plant have the highest rate of N xation [27]. In this
symbiotic relationship, the N xer is maintained by the plant and
uses the plant as a carbon resource, while returning xed N to plant
by root excretion and litter decomposition [1,27]. Despite high
mineral N pools in soils, a summary of 12 eld studies reported that
rates of BNF ranged from 15 to 36 kg N hm2 year1 in tropical forests,
with the majority of BNF attributed to symbiotic bacteria in root
nodule [27]. In addition, free-living microbes in litter and soil can
also contribute sizeable uxes of N via BNF in tropical ecosystems
[28,29]. The BNF rates in tropical forests are similar to or even higher
than that estimated in temperate forests (727 kg N hm2 year1) [27].
Houlton et al. [30] indicated that BNF in temperate forest provid-
ed N to plant growth, but the high rates of BNF in tropical forests
were required to maintain for the production of soil enzymes (es-
pecially for phosphatases) to acquire phosphorus (P) or other limiting
nutrients.
The nutrients assimilated by plant (above 90% of N and P, 60% of
other mineral elements) mainly come from litter decomposition in
many forest ecosystems. To some extent, the rate of litter decom-
position determines nutrient cycling and soil N availability in forest
ecosystems [31]. As microorganisms break down dead organic matter
(from plants, animals, and microbes) during decomposition, the N
and P are released as dissolved organic matter (DOM) by the action
of exoenzymes. And then the DOM is mineralized to mineral forms
that can be used by plant and microorganisms [1]. Physical envi-
ronment, quantity and quality of substrates, and microbial community
characteristics are the factors to control litter decomposition in forests
[32]. At global and regional scales, the climate conditions (temper-
ature, precipitation, etc.) are the crucial factors to control
decomposition, while litter qualities (litter C and N content, lignin
content, C/N ration, etc.) limit litter decomposition at local scales.
Litter C/N, N/P and lignin/N ratios are considered to predict litter
decomposition and nutrient dynamic [33,34].
37
Nitrogen oxide emission 7
Dentrification5
Assimilation
Soil NH4+-N pool Soil NO3--N pool
Nitrification 4
Immobilization
Microbial biomass N pool NO3--N leaching 8
1.2. Soil N transformation
Most soil N stores in dead organic matter and can be converted
from insoluble organic nitrogen to dissolved organic N (DON) by
microorganisms in natural forest ecosystems. In order to relieve C
limitation, microbes break down the DON, use the C skeleton to
support their energy requirements for growth and maintenance, and
secrete NH4+ into the soil [1]. This process is termed nitrogen min-
eralization or ammonication [1]. Part of NH4+ is assimilated by plant,
immobilized by microbial, or absorbed by clay minerals. The other
part of NH4+ is oxidized to (NO2) and then to nitrate (NO3) by ni-
trifying bacteria. The conversion from ammonium to nitrate is termed
nitrication [1]. The H+ cation is produced during nitrication, which
possibly cause soil acidication. NO3 is prone to loss from ecosys-
tem by leaching or N oxide emissions [35]. Some 15N isotope tracing
experiments showed that there was a close relationship between
mineralization and nitrication in forests [36,37]. Gilliam et al. [38]
reported that 90% of NH4 produced by ammonication is con-
verted to NO3.
Denitrication is a process that nitrate or nitrite was reduced
to N2O or N2 by denitrifying bacteria; denitrication is also an im-
portant pathway to balance ecosystem N budget. In general, N losses
through denitrication are low in natural forest ecosystems [1,2].
The rates of denitrication are far below 1 kg N hm2 year1 in the
N-limited forests [15,39]. The emissions of N 2 O are less than
2 kg N hm2 year1 even in the N-rich tropical forests [6,10,17]. Long-
term elevated N deposition is expected to increase N2O and NO
emissions to atmosphere by accelerating the rates of nitrication
and denitrication in forest ecosystems.
1.3. Soil N output
N can lose from soils in the avenues of gas forms in forest eco-
systems, including NH3, NOx and N2O. N2O is one kind of long-lived
greenhouse gases with an atmospheric lifetime of 114 years. Its po-
tential of global warming for one hundred year is 298 times comparing
to CO2. N2O also contributes to the depletion of stratospheric ozone
[40]. NO is an active gas that impacts on climate through the pho-
tochemical formation of tropospheric ozone. NO is also an important
substance to induce acid rain [41]. N2O and NO are by-products from
nitrication and denitrication. The N-oxide emissions depend on
nitrication, NO3 concentration, low oxygen condition, and supply
of organic C [1,42]. Tropical rain forests (N-rich) usually have higher
rate of nitrication than temperate forests (N-limited), and emit more
N-oxide to atmosphere [17,21]. Elevated N deposition is expected
to further aggravate soil N-oxide emissions in these forests [17,21].
NH3 volatilization is another avenue of gaseous N loss from eco-
system, and has a strong relation to soil conditions. A model of NH3
38 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543
volatilization in soil showed that NH3 ux depended on soil pH values
and cation exchange capacity [43].
NO3 and dissolved organic N (DON) account for most of the so-
lution loss from ecosystems [1]. Undisturbed temperate ecosystems
that receive low N deposition generally have relatively little N leach-
ing, and most N can immobilize by plant and microbes. N leachate
in these forests is primarily DON [44,45]. Tropical rainforests grown
on heavily weathered soil show a lack of N limitation on net primary
productivity (NPP) due to high mineral N content in soil. Thus these
forests have high potential of N leaching [46]. Lewis et al. [47] found
that NO3 accounted for above 80% of DIN output in tropical wa-
tersheds. Elevated N deposition is expected to increase soil NO3
leaching in tropical and subtropical forests.
2. Study methods for the effect of N deposition on soil N cycle
in forests
Effects of N deposition on soil N cycle have been studied in many
tropical, subtropical and temperate forests. Methods of simulated
N deposition experiments, N-deposition gradient, N input manip-
ulation and 15N isotope tracing were used to study the effect of N
deposition on soil N cycle. These methods are briey introduced as
follows (Table 1):
(1) Long-term simulated N deposition experiments. Sampled plots
were established in various forest types to examine the re-
sponses of soil N cycle to different doses and forms of N
fertilizer (NH4NO3, NaNO3, (NH4)2SO4 or urea). For examples,
NITREX program, the Harvard forest and the Bear Brook wa-
tershed, Hawaiian tropical forests, Luquillo forests, and the
DHSBR [9,13,1517,19]. This method permits us to assess the
real responses of ecosystem to simulated N deposition by con-
trolling the dose and length of N fertilization [2]. However,
a limitation of this method is that long-term study is needed
(possible several years), because the responses of forest eco-
systems to N addition cannot completely reveal in a short time.
Such as NITREX and EXMAN, both of these two experi-
ments have lasted more than 15 years. In China, the simulated
N deposition experiment in DHSBR has been conducted for
more than 10 years.
(2) N-deposition gradient method. Forest ecosystems with various
levels of background N deposition were selected to compare
their pattern of N cycling. NITREX and EXMAX programs in
Europe examined the responses of coniferous forests
to different levels of background N deposition (2.6
59 kg N hm 2 year 1 ) [13,14]. Mnsson and Falkengren-
Grerup [48] determined the N mineralization, nitrication and
litter C/N ratio of two forests receiving different levels of N
deposition (17 and 10 kg N hm2 year1) in southern Sweden.
The advantage of this method is the study time can be short-
ened, but the interferences of forest heterogeneity (for
examples, the regional climate, geographical position, plant
composition, soil properties and land use history) are di-
cult to be eliminated.
(3) N input manipulation method. A roof manipulation is applied
to determine whether the N saturation of ecosystems can
be reversed after reduced N deposition. Meanwhile, the eco-
system N cycling in the absence of N deposition in the pass
can be assessed by this method [49]. Because the roofs also
clear the precipitation at the same time, equal deionized water
must be added to the plots, which cause anthropogenic
disturbances.
(4) 15N isotope tracing method. The 15N isotope tracing method is
applied to examine the changes of N allocation (plant, micro-
organism and soil), transformation and uxes (mineralization,
nitrication, N oxide emission, NO3 leaching). For examples,
the Solling plateau forests in Germany, the La Selva Biologi-
cal Station in Costa Rica, the Barro Colorado Nature Monument
in Panama [6,21,49].
3. The effect of N deposition on soil N cycle in forests
3.1. The effect of N deposition on soil N input
3.1.1. Effects of N deposition on BNF
BNF and N deposition are two major pathways for N input in
many terrestrial ecosystems, but their relationship is less as-
sessed. Atmospheric N2 can be xed in forest oor, mineral soil,
mosses, lichens, and canopy epiphylls by diazotrophs, and then this
part of N will participate in N cycling in forest ecosystems [55].
Cusack et al. [55] estimated the rates of BNF for two tropical forests
and their responses to increased N availability by measuring nitro-
genases activity. They indicated that the rates of background BNF
were approximately 12.3 2.7 kg N hm2 year1 in the lower eleva-
tion forest, and 8.4 1.4 kg N hm2 year1 in the upper elevation forest;
N addition signicantly inhibited BNF in mineral soil (010 cm) and
forest oor in these two forests [55]. Barron et al. [58] reported that
fertilization with N (urea, 125 kg N hm2 year1) caused a ~75% de-
crease in nitrogenases activity in tropical forests in Panama. Isaac
et al. [59] found that nodule numbers on Acacia Senegal roots under
solution with N (about 89) were signicantly smaller than that
grown in an N-free solution (about 18), indicating a signicant de-
crease in the number of nodules when N was added in solution in
the form of NO3 compared to N-free solution. Walker and Syers [60]
indicated that when soil N storage exceeded a certain amount, and
N was no longer the most crucial limited factor, symbiotic N xers
would lose their competitive advantages in growth or be excluded
from plant communities.
3.1.2. Effects of N deposition on litter decomposition and nutrient
dynamic
N deposition is expected to affect soil N cycling directly by im-
proving available N, and also affects the rate of nutrient input
indirectly by altering litter decomposition and nutrient release. Knorr
et al. [61] observed that the effect of N addition (N deposition) on
litter deposition depended on site-specic ambient N deposition
level, fertilization rate, and litter quality. Litter decomposition was
inhibited by N additions when fertilization rates were 220 times
higher than the anthropogenic N deposition level, when ambient
N deposition was 510 kg N hm2 year1, or when litter quality was
low (typically high-lignin litters). Whereas litter decomposition was
stimulated at eld sites exposed to low ambient N deposition
(<5 kg N hm2 year1), and with high-quality (low-lignin) litters. Ac-
cording to the related studies in temperate and tropical forests, we
concluded that short-term N deposition was expected to stimu-
late the rate of litter decomposition and nutrient turnover in the
N-limited temperate forests [6264], however, the rate of litter de-
composition would decrease in long-term N deposition due to N
limitation was relieved [65,66]. Conversely, in the N-rich tropical
and subtropical forests, N deposition has negative or neutral effect
on litter decomposition due to higher litter N content and soil N
availability [56,67].
Parton et al. [68] studied the net N immobilization and release
of decomposing litter with different initial N concentrations, and
found that net N immobilization and mineralization of decompos-
ing litter were strongly limited by initial tissue N concentration; net
N release started when the average C/N ratio of leaf litter is less than
40. Moore et al. [69] examined the patterns of N and P dynamic
during decomposition in ten foliar tissues over 6 years at 18 upland
forests in Canada; they found that net N release started when the
average C/N ratios of leaf litter are less than 55 and litter accumu-
lated more N in the sites with high soil N availability. The changes
Table 1
Various researches of the responses of forest ecosystem to N deposition in tropical, subtropical and temperate zone.

Zone Study sites Forest types Study methods Background N Treatment Study contents References
deposition (kg N ha1 yr1)
(kg N ha1 yr1)

Temperate forests Grdsjn (GD) Sweden;
Klosterhede (KH), Denmark;
Aber (AB), Wales, UK; Speuld
(SP) and Ysselsteyn (YS), the
Netherlands
Harvard forest, Massachusetts,
USA (4230N, 7210W)
Bear Brook watershed, Mains,
USA (4452N 6806E)
Skane and Smland, Southern
Deciduous mixed N-deposition gradient;
coniferous and
broad-leaved forests
Red pine plantation; mixed
hardwood stand
Hardwood and softwood
stand
Deciduous broad-leaved
1359 GD, KH, AB :0, 33; SP, Decomposition, soil net (potential) N Gundersen et al. [13]
N addition; 15N tracing YS: N removal transformation, denitrication, root
biomass, dissolved organic C and N
N addition 8 0, 50, 150 NO, N2O emission; total dissolve N Magill et al. [15]; Venterea
(TDN), dissolve organic N (DON), et al. [42]
dissolve inorganic N (DIN) in soil
solution, soil total C and N content,
foliar chemistry; litterfall, wood
biomass, ne roots
N addition 8.4 West Bear: 25 Soil net nitrogen mineralization and Jefts et al. [16]
East Bear: 0 net nitrication
N-deposition gradient 17, 10 Carbon and nitrogen mineralization, Mnsson et al. [48]

X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543

Sweden
Sollingplateau, German
(5146N,934E)
Cedar Creek Ecosystem Science
Reserve, Minnesota, USA
(4540N, 9320E)
Klosterhede, Western Juland,
Denmark (5429N, 824E)
Grdsjn, Sweden(5840N,
1230E)
Changbai mountain, China
(4024N, 1286E)
San Bernardino Mountains,
California, USA
Tropical and Gigante Peninsula (906N,
subtropical 7748E) and Quebrada Honda
forests area (845N, 1316E), Panama
Luquillo Experimental Forest,
Puerto Rico (183N, 658E)
Hawaii, USA
La Selva Biological Station,
Costa Rica (1026N, 8359W)
Dinghushan Biosphere Reserve,
southern China (2310N,
11210E)
Guanzhuang National Forestry
Farm, South China (2630N,
11743E)
forest (oak forest) nitrication, litter C/N ratios
Beech and spruce forest N-deposition gradient; 20, 33 CK, Removal 65% of N NO, N2O emission; gross nitrogen Eickenscheidt et al. [39]
N removal; 15N tracing deposition in mineralization and gross nitrication, Corre and Lamersdorf [49]
throughfall N immobilization, net nitrication, N
leaching
Eight upland sites N addition 5.6 0, 100 Litter decomposition and N dynamic Hobbie et al. [50]
Spruce plantation N addition; 20 0, 35 Tree growth, ground vegetation, litter Gundersen [51]
15Ntracing production and decomposition,
mineralization and nitrication
Coniferous forest N addition 9 41 Nitrogen leaching; acidication Moldan and Wright [52]
Korean pine forest; N addition 45 Dissolved N2O and CO2; dissolved Xu et al. [53]
broadleaf mixed forest organic matter; inorganic nitrogen in
soil solution
Pine mixed forest N-deposition gradient; 8.3, 81.6 0, 50, 150 Nitrogen mineralization and Fenn et al. [54]
N addition nitrication
Old-growth semi- N-deposition gradient; 3, 9 0, 125 (the lowland Gross N mineralization and Corre et al. [21]
deciduous forest; old- N addition; 15N tracing site) nitrication, N immobilization rates,
growth montane forest N-oxide emission
Wet tropical rainforest; N addition 7.2 0, 50 Microbial community characteristic, Cusack et al. [19,55]
montane rainforest soil organic matter; biological nitrogen
xation
Three montane rainforests N addition 0, 50, 100 (for YS in Nitrate solution losses, soil inorganic N Hall and Matson [17]
(NPP limited by N to P) 1985 and OS for1991) pool, N transformation rates, N2O and
NO emission
Plantation, old-growth N addition; 15N tracing 320 (only in Gross N cycling, microbial N Silver et al. [6]
forest plantation) assimilation, dissimilatory nitrate
reduction (DNRA) and nitrous oxide
uxes
Evergreen broadleaf forest; N addition 34.2 0, 50, 100, 150 N leaching; litter decomposition; soil Fang et al. [9];
mixed forest; pine forest inorganic N dynamic Li et al. [10];
Mo et al. [56]
Chinese r plantation N addition 4257 0, 60, 120, 240 Soil microbial community, understory Wu et al. [57]
plant community

39
40 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543
of litter initial N content, litter C/N ratio, and soil N availability caused
by N deposition, may affect the pattern of N immobilization and min-
eralization. Perakis et al. [63] examined relationships between initial
N concentration (0.671.31%), decomposition, and N dynamics in
both ambient and N fertilized (150 kg N hm2 year1) plots at four
Douglas r forests over 3 years. They found that litter with low initial
N concentration immobilized N strongly during decomposition,
whereas litter with high initial N concentration immobilized less
N in both the control and N fertilized plots. Hobbie and Vitousek
[70] also proved that N addition increased net N immobilization in
decaying low initial-N litter.
3.2. The effect of N deposition on soil N transformation
The responses of soil N mineralization and nitrication to N de-
position depend on N status, dose and length of N fertilization, and
soil quality in forest ecosystems. Some researches showed that N
deposition (or N addition) stimulated soil N mineralization and ni-
trication. Gundersen et al. [13] examined rates of N transformation
in O horizon at ve coniferous forests with different levels of N de-
position (1354 kg N hm2 year1) and found that net N mineralization
in O horizon was increased (1851727 mg N km2 year1) follow-
ing the N deposition gradient. Gross N mineralization and net N
mineralization showed a good consistency. However, N nitrica-
tion was detected only in forests receiving high N deposition. There
was a close relation among mineralization, nitrication and N de-
position [13]. Mnsson and Falkengren-Grerup [48] also found that
the rate of soil net N mineralization and nitrication were higher
in the forest receiving high N deposition (17 kg N hm2 year1) than
the one receiving low N deposition (10 kg N hm2 year1). Magill et al.
[71] detected the soil N dynamic at Harvard forest (deciduous and
coniferous forest) receiving long-term N addition in the U.S., and
reported that the response of soil nitrication to N addition in the
coniferous forest was more sensitive than that in the deciduous
forest. This result indicated that the deciduous forest had higher ca-
pacity of N retention than the coniferous forest, due to variances
in heterotrophic microbial assimilation, abiotic immobilization, my-
corrhiza uptake, and land use history. A N addition experiment in
the Bear Brook watershed showed that N addition signicantly in-
creased the potential net N mineralization in O horizon, as well as
the (potential) net N nitrication in both O horizon and mineral soil
[16]. Corre et al. [21] used N-addition experiments to achieve
N-enriched conditions in mixed species, lowland and montane forests
in Panama. In lowland forest, soil N mineralization and nitrica-
tion appeared to have a signicant increase after 9-year N addition.
Meanwhile, the capacity of soil and microbes to immobilize N was
decreased in this forest. But in montane forest, 1-year N addition
signicantly increased soil mineralization and nitrication, and mi-
crobial NH4+ immobilization. These results implied that the responses
of soil N transformation to N addition depended on forest N status.
The lowland forest had rapid rate of N turnover, so 1-year N addi-
tion had no effect on soil N transformation in this forest [21].
However, others studies showed that N deposition (N addi-
tion) reduced rates of soil N transformation. Corre and Lamersdorf
[49] reported that an apparent decrease in gross N mineralization,
lower microbial NH4+ immobilization rates, and higher NO3 leach-
ing for a N-saturated spruce stand receiving long-term high
throughfall N deposition (total N input of 41 kg N hm2 year1) in
Solling, Germany. By an ongoing roof experiment, they found that
long-term reduction of throughfall N deposition had a large con-
tribution to the reversal of N saturation in this forest [49]. An N and
P addition experiment at three tropical forests with different nu-
trient statuses (N limitation, NP combined limitation, and P
limitation) in Hawaii showed that only high doses of N (125 and
175 kg N hm2 year1) resulted in net positive rates of soil N min-
eralization and nitrication in N-limited forest. Inversely, long-term
N addition did not signicantly alter soil N availability and miner-
alization in NP-limited and P-limited forests, due to high background
soil N availability and gross (and net) N mineralization. They also
found that long-term addition in the P-limited forest caused a sig-
nicant increase in the number and/or activity of nitrifying
microorganism [17].
3.3. The effect of N deposition on soil N output
The response timing and magnitude of soil N losses to N addi-
tion depend on ecosystem N status [21]. N-limited forests usually
have less N losses (NO3 leaching or N-oxide emissions) because of
intensive competition between plant and microbes (nitriers).
However, when the ecosystem reaches N saturation, N losses will
accelerate [8]. In the Bear Brook watershed, the stream export in
West Bear (total deposition + treatment: 36 kg N hm2 year1) was
24 times higher than that in East Bear (background N deposition:
8 kg N hm2 year1); the stream exports in these two watersheds were
7.3 and 0.3 kg N hm2 year1, respectively [15]. In addition, a whole-
catchment experiment with N addition (41 kg N hm2 year1) has been
conducted at Grdsjn, Sweden to investigate the risk of N satu-
ration early in 1991. The result of this experiment showed that the
fraction of input N lost to runoff had increased from 0% to 10% [52].
Tropical and subtropical forests grown on highly weathered soils
are considered to have higher biologically available N and faster rate
of N turnover than that in the temperate forests. In tropical forests,
NPP is likely to be limited by P or other rock-derived nutrients [72,73].
It is possible that elevated N deposition will result in larger and more
immediate losses of N as soil N-oxide emission or NO3 leaching in
these forests [46]. Hall and Matson [17] indicated that N-oxide emis-
sions were negligible following rst-time N additions in N-limited
forest, and they increased signicantly following 11-year N fertil-
ization. In contrast, N-oxide emissions were large after both rst-
time and long-term N fertilization in NP-limited and P-limited forests.
Corre et al. [21] suggested that the response of soil N-loss to el-
evated N input depended on soil mineral N production and retention
but not on whether plant limited by N in tropical forests [21]. Ac-
cording to their research in Panama, there was no immediate effect
during the rst-year N addition (125 kg N hm2 year1) on gross rates
of mineral-N production and N-oxide emissions in the lowland forest
(non-N-limited). Only in the chronic (9 year) N-addition plots,
N-oxide emissions and NO 3 leaching increased signicantly
(196 g N m2 day1, 1498 g N m2 day1, 0.93 mg N L1 for N2O,
NO2 and NO3N, respectively), compared to the control plots
(70 g N m2 day1, 448 g N m2 day1, 0.01 mg N L1). In contrast, rst-
year N addition signicantly increased N-oxide emissions and NO3
leaching in the montane forest (N-limited). In the N-addition plots,
N-oxide emissions and NO 3 leaching were 66 g N m 2 day 1 ,
658 g N m2 day1, 0.14 mg N L1, compared to 28 g N m2 day1,
326 g N m2 day1, 0.03 mg N L1 in the control plots [21]. Fang et al.
[9] found that N leaching signicantly increased after 1.5-year N ad-
dition in two forests (Pine forest and monsoon broadleaf forest),
accounting for 2566% of the annual amount of N addition. The values
of N leaching in these two forests were higher than that reported
in temperate forests in Europe and North America. These results
suggest that elevated N deposition may increase the risk of N leach-
ing in subtropical forests in China. So it is important to explore the
responses of these N-rich forests to elevated N deposition and the
related mechanisms.
4. Mechanisms for N deposition effects on soil N cycling
4.1. Altered litter and forest substrates chemical qualities
N deposition eciently improved soil N availability, as a result
plant can assimilate N from soil more easily. This part of N is allocated
 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543
to each tissue, causing an increase in tissue N concentration. Mean-
while plant also assimilates others nutrients (such as P, Ca, Mg) from
external environment to keep it own elemental balance [74]. As the
result of lower C/N and C/P ratios of litter and forest oor, mi-
crobes can consume fewer resources to decompose these materials,
which in turn accelerated the decomposition rate. However, Perakis
et al. [63] found that the positive effect of N addition on decom-
position only appeared in the early stage (0.67 year), the negative
effect appeared after 3-year decomposition (mass remaining was
54.6% in the control plots and 62.2% in the N-addition plots). In ad-
dition, many other studies also proved that N addition (N deposition)
inhibited litter decomposition in the later stage or soil organic matter
decomposition [66,75]. One possible reason for this result is that
the added-N combined with lignin and phenolic matter to form more
recalcitrant materials to start the rst stage of humication earlier
[34,76].
There is a close relation between N mineralization rate and sub-
strate C/N ratio. In general, substrates with high C/N ratio show low
rate of N mineralization. The critical value of substrate C/N ratio
between immobilization and mineralization is considered to be 25.
When C/N > 25, microbes immobilize N from environment because
microbial growth is limited by N. On the contrary, when C/N < 25,
N mineralization begins as a result of microbial growth is limited
by C and N is relatively sucient [77].
4.2. Altered plant biomass and the structure of communities
External N addition, on the one hand, relieved N limitation of
NPP, and improved litter production and litter quality (initial N
content) in N-limited forest ecosystems [78]. On the other hand, N
deposition affected the microenvironment of litter decomposition
(such as the surface temperature and humidity) by altering forest
canopy density and understory growth [79]. Moreover, N deposi-
tion possible change the BNF of mosses, canopy epiphylls, and lichens
by altering their biomass and community composition [58]. N de-
position rst reaches forest canopies, and large amount of N is
intercepted by canopy epiphylls in mature tropical forests [80]. The
response of leaf chemical characteristics of forest canopy is sensi-
tive to N deposition, which may lead to reduction of epiphytic BNF
[81]. Stemow acidication caused by N deposition altered the
biomass and community composition of tree mosses and lichens,
and then reduced their BNF capacity. Meanwhile, soil acidication
changed the understory community, which weakened soil N re-
tention and increased the risk of N losses in these forests [57,82].
4.3. Changed the activity and composition of microbial communities
Soil microbes are the main decomposers in forest ecosystems;
their quantity, community structure, and activity are important
factors that affect forest litter decomposition. N deposition direct-
ly supplies plenty of N to microbial growth, and microbes can invest
more N to product N-rich enzymes that results in an acceleration
in decomposition rate [83]. In addition, the competition between
nitries, plant, and others microbes are relieved by improved N avail-
ability. The rates of N nitrication, denitrication and the potential
risk of NO3 leaching are increased by external N input [8,13,84].
However, N deposition can reduce the rate of litter decompo-
sition by changing the ratio of fungi/bacteria and suppressing the
synthesis of soil enzymes [85]. Fungi play a crucial role in decom-
position and mineralization in boreal forest ecosystems, because they
can bear acid environment and decompose recalcitrant material
[86,87]. Excess N input decreased fungi biomass and converted the
microbial community from fungi-dominant to bacteria-dominant
[88]. The reduction of fungi species is an important reason for the
decrease of litter decomposition and the acceleration in nitrica-
tion and NO3 leaching. Moreover, high N input also decreased the
41
activity of white-rot fungi and inhibited the synthesis of ligninolytic
enzymes [83,89].
5. Problems and prospects
Soil N cycle in forests is a complex process that when N input
to the ecosystem, its uxes and fate are controlled by various biotic
and abiotic factors. Present researches prove that different forest
types show different response timing and patterns of N cycle to N
deposition. Our understanding of N cycle and its response to N de-
position is still limited. It is meaningful to explore the effect of N
deposition on forest N cycle and its relative mechanisms.
5.1. Differences between regions
The effect of N deposition on forest ecosystems has been studied
in Europe and the U.S. early in the 1980s. Most of these studies chose
coniferous forests as study object, and their conclusions were just
universal in temperate forest ecosystems where N is the limited
factor for NPP. However, in tropical and subtropical forests, NPP is
limited by rock-weather depleted elements (such as P and Ca), but
not by N. Therefore, the potential N losses in these forests are higher
than that in temperate forests [46,72,73]. Researches on the effect
of N deposition on forest ecosystems in tropics and subtropics were
carried out later than that in the temperate forests. The sampled
sites are few and the length of study is short in tropical forests. Long-
term study is lack, whereas some response of forest components
to N addition occurs after many years of N deposition (or N addi-
tion). In China, the different responses of soil N cycle to N deposition
and their mechanisms between the southern and the northern forests
cannot be compared because most of the existing reports focused
in subtropical forests in DHSBR, and less can be found in other places.
It is important to realize the ecological and environmental issues
caused by N deposition, which provides theoretical references on
developing related policy and taking action to limit the negative N
effects.
5.2. Changes of forest type
According to Global Forest Resources Assessment 2010, the area
of plantations has increased at the rate of 5.0 108 ha yr1 and oc-
cupied about 2.64 108 ha worldwide until 2010 [90]. Afforestation
is a major method in rehabilitating degraded tropical ecosystems
[91]. This change of forest land cover certainly impacts the re-
sponse of soil N cycle to N deposition. However, most results
mentioned earlier came from primary forests; less attention has been
paid to plantations. To clearly understand the effect of elevated N
deposition on soil N cycle in plantations can provide the scientic
reference on tree species selection and forest management for af-
forestation or reforestation in the regions receiving high N deposition.
5.3. Limitations of study
As mentioned earlier, forest soil N cycle is a complex process
involving various biotic and abiotic factors. Our knowledge of the
mechanisms in soil N retention is still incomplete; only a few
reports introduced the role of plant and microorganisms played
in ecosystem N retention [6,7]. Microbial N immobilization, trans-
formation, and release can partly explain the fate of N deposition,
and determine the rate of soil N cycling. However, due to the
limitation of research funding and techniques, many studies used
the in-situ soil core incubation to study soil nitrogen transforma-
tion, and less adopted the 15N isotope tracing method to trace the
fate of added N.
42 X. Zhu et al./Acta Ecologica Sinica 35 (2015) 3543
5.4. Relationships between C, N and P
N deposition increased ecosystems C sequestration by increas-
ing the growth of plant and microorganisms that had a signicant
effect on the regional or global C cycling. It is meaningful to explore
the changes of C and N cycling with the background of elevated
global CO2 and N deposition [92]. N and P are two key factors to
limit NPP in terrestrial ecosystems. N deposition improved N status
in N-limited forests, leading to N saturation and P limitation [93].
The alterations of stoichiometric ratios of C, N and P in various eco-
system components induced by elevated N deposition, and their
impacts on ecosystem processes have received more and more
attentions.
Acknowledgements
This study was nancially supported by National Natural Science
Foundation of China (No: 41273143, 31000236) and the National
Key Basic Research Program (2010CB833502). We also thank several
anonymous reviewers whose comments improved the quality of this
manuscript.
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