Biogeosciences, 10, 1083–1095, 2013
www.biogeosciences.ne /10/1083/2013/
doi:10.5194/bg-10-1083-2013
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Ni ogen balance o a bo eal Sco s pine o es
J. F. J. Ko honen1, M. Pihla ie1, J. Pumpanen2, H. Aal onen2, P. Ha i2, J. Le ula3, A.-J. Kieloaho1, E. Nikinmaa2,
T. Vesala1, and H. Il esniemi4
1Depa men o Physics, Uni e si y O Helsinki, P.O. Box 48, 00014, Helsinki, Finland
2Depa men o Fo es Sciences, Uni e si y O Helsinki, P.O. Box 27, 00014, Helsinki, Finland
3Hyy i¨
al¨
a Fo es y Field s a ion, Hyy i¨
al¨
an ie 124, 35500, Ko keakoski, Finland
4Finnish Fo es Resea ch Ins i u e, Van aa Uni , P.O. Box 18, 01301, Van aa, Finland
Co espondence o: J. F. J. Ko honen ([email p o ec ed])
Recei ed: 20 July 2012 – Published in Biogeosciences Discuss.: 20 Augus 2012
Re ised: 11 Decembe 2012 – Accep ed: 14 Janua y 2013 – Published: 15 Feb ua y 2013
Abs ac . The p oduc i i y o bo eal o es s is conside ed
o be limi ed by low ni ogen (N) a ailabili y. Inc eased a -
mosphe ic N deposi ion has al e ed he unc ioning and N
cycling o hese N-sensi i e ecosys ems by inc easing he
a ailabili y o eac i e ni ogen. The mos impo an com-
ponen s o N pools and luxes we e measu ed in a bo eal
Sco s pine s and in Hyy i¨
al¨
a, Sou he n Finland. The measu e-
men s a he si e allowed di ec es ima ions o nu ien pools
in he soil and biomass, inpu s om he a mosphe e and ou -
pu s as d ainage low and gaseous losses om wo mic o-
ca chmen s. N was accumula ing in he sys em, mainly in
woody biomass, a a a e o 7kgNha−1y −1. Ni ogen in-
pu as a mosphe ic deposi ion was 7.4kgNha−1y −1. D y
deposi ion and o ganic N in we deposi ion con ibu ed
o e hal o he inpu s in deposi ion. To al ou pu s we e
0.4kgNha−1y −1, he mos impo an ou pu s being N2O
emission o he a mosphe e and o ganic N lux in d ainage
low. Ni ogen up ake and e ansloca ion we e equally im-
po an sou ces o N o plan g ow h. Mos o he assim-
ila ed N o igina ed om decomposi ion o o ganic ma e ,
and he ac ion o N ha could o igina e di ec ly om de-
posi ion was abou 30%. In conclusion, a mosphe ic N de-
posi ion e ilizes he si e conside ably, bu he e a e no signs
o N sa u a ion. Fu he esea ch is needed o es ima e soil
N2 luxes (emission and ixa ion), which may amoun up o
se e al kgNha−1y −1.
1 In oduc ion
An h opogenic emissions o eac i e ni ogen (N) ha e
ma kedly inc eased he a mosphe ic N deposi ion o o es s,
especially a ound indus ialized egions (Pinho e al., 2012;
G ube and Galloway, 2008; Galloway e al., 2003). The e
is, howe e , a la ge spa ial a iabili y in he e ec s by N
deposi ion (Magnani e al., 2007; Fische e al., 2010). Fo -
es ecosys ems wi h slow N cycling and low o mode a e a -
mosphe ic N deposi ion a e called ni ogen limi ed, as hei
p oduc i i y is enhanced by he inc eased N inpu s. Fo -
es ecosys ems wi h high deposi ion a es ecei e N in ex-
cess, which inc eases he ou pu s ma kedly. In such a case
he ecosys ems a e called ni ogen sa u a ed (Abe e al.,
1998). He e we di ide N cycling in o es s in o inpu s, ou -
pu s and in e nal cycling. Inpu s include a mosphe ic N de-
posi ion, ixa ion, and e iliza ion. Ou pu s include N losses
in gaseous emissions and d ainage low. In e nal cycling in-
cludes all he p ocesses whe e N is anspo ed wi hin he
ecosys em. The inpu s and ou pu s o N o and om undis-
u bed o es ecosys ems a e small, and he in e nal cycling
domina es he N low (M¨
alk¨
onen, 1974). The inc eased N de-
posi ion in u n a ec s he whole N-cycling p ocess in o es
ecosys ems.
In bo eal o es s, he inpu s o N ia a mosphe ic de-
posi ion and N2 ixa ion a e ela i ely small, a maximum
a ound 10kgNha−1y −1(Flecha d e al., 2011; Sy i e al.,
2004; Mus aj¨
a i e al., 2008) and 0.1–3.5kgNha−1y −1
(DeLuca e al., 2002, 2008; Zack isson e al., 2004, 2009),
espec i ely. In hese sys ems, he N ou pu s a e epo ed o
be small, bo h ia leaching o ammonium (NH+
4-N), ni a e
Published by Cope nicus Publica ions on behal o he Eu opean Geosciences Union.
1084 J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es
(NO3-N) and dissol ed o ganic ni ogen (DON) in o g ound-
wa e (Kubin, 1998), and h ough ola iliza ion o oxidized
ni ogen (N2O, NOx)in o he a mosphe e (Pilegaa d e al.,
2006; Pihla ie e al., 2007; Maljanen e al., 2010). The soil
emissions o N2a e highly unce ain as he e a e no measu e-
men s a ailable om bo eal ecosys ems. In gene al, he o al
N inpu s and ou pu s in bo eal o es s a e ma kedly less han
hose in mo e N-a ec ed Cen al Eu opean o es ecosys ems
(Flecha d e al., 2011; Holland e al., 2005). In bo eal o es s,
N is epo ed o accumula e in o he soil (Be g and Dise,
2004; Ha enschwile and Vi ousek, 2000) and biomass o
g owing ees.
Acco ding o he cu en knowledge, plan s can ake up N
ei he in mine al (NH+
4o NO−
3)o amino acid o ms (e.g.
Kielland e al., 2006). Ni ogen up ake by plan s is a ec ed
by he a ailabili y o hese compounds, eleased ia decom-
posi ion, bu also by he a mosphe ic N deposi ion and N2
ixa ion. E en hough he e a e la ge pools o N in he bo eal
ecosys ems, he e is less N a ailable o plan up ake han
plan s a e able o consume. This is concluded om he ac
ha N e iliza ion ends o inc ease he p oduc i i y o bo-
eal o es s (Saa salmi and M¨
alk¨
onen, 2001). In bo eal up-
land o es s, he low N a ailabili y esul s om he cool cli-
ma e and he chemical composi ion o soil o ganic ma e .
Howe e , plan s can euse N e icien ly because i is a mobile
nu ien . A majo ac ion o he N ha is being los in senesc-
ing plan issue can be eso bed and e ansloca ed when new
issue is g own.
As se e al s udies ecognize, he ole and magni ude o
o ganic N inpu s o and ou pu s om he ecosys ems and di-
ec plan up ake has la gely been o e looked (Kielland e
al., 2007; Ne e al., 2002; Mus aj¨
a i e al., 2008). Recen
s udies show ha o ganic N can con ibu e as much as 30%
o he o al N deposi ion in o ecosys ems (Ne e al., 2002),
and up o 80% o he o al N los as uno (Mus aj¨
a i e
al., 2008). I seems e iden ha ees up ake N om soil di-
ec ly as amino acids (Jones and Kielland, 2002; Kielland e
al., 2007).
He e we p esen a measu emen -based N budge o a bo-
eal Sco s pine o es in Sou he n Finland. We show he N
budge based on a comp ehensi e da a se ies co e ing he
inpu s, ou pu s, pools, and in e nal cycling o N wi hin he
o es ecosys em om 2006 o 2010. We u he calcula e
he indi idual sou ces o N o he plan s and he o al N
a mosphe ic deposi ion. The s udy complimen s he long-
e m measu emen s o ca bon and wa e balances o he si e,
which a e p esen ed in Il esniemi e al. (2009, 2010), espec-
i ely.
2 Ma e ials and me hods
2.1 Measu emen si e
Measu emen s we e conduc ed a a Sco s pine s and a he
SMEAR II s a ion in Hyy i¨
al¨
a (Ha i and Kulmala, 2005),
Sou he n Finland (61◦510N, 24◦170E). The mean annual ai
empe a u e and p ecipi a ion a Hyy i¨
al¨
a om 1971 o 2000
we e 3.3◦C and 713mm, espec i ely (D ebs e al., 2002).
The s and is an e en-aged o es , and i was egene a ed
by sowing a e clea -cu ing, p esc ibed bu ning, and soil
p epa a ion in 1962. The measu emen s a ion was es ab-
lished in 1995. The s and was pa ially hinned om Janua y
o Ma ch 2002 (Vesala e al., 2005).
The dominan ee species is Sco s pine, co e ing 93%
o he s em basal a ea in he s udy a ea. O he o he ee
species, mainly in he unde s o ey, he mos impo an a e
No way sp uce (Picea abies) and Sil e bi ch (Be ula pen-
dula), con ibu ing 2.6% and 1.1% o he o al basal a ea,
espec i ely. O he species in he unde s o ey include owan
(So bus aucupa ia), G ey alde (Alnus incana), Goa willow
(Salix cap ea) and Eu asian aspen (Populus emula). The
dominan species in he ield laye a e he sh ubs Vaccinium
my illus and Vaccinium i is-idaea, and in he g ound laye
he mosses Dic anum polyse um and Pleu ozium sch ebe i
(Kulmala e al., 2008).
The soil a he si e is Haplic podzol on glacial ill (FAO-
UNESCO-ISRIC, 1988), o e laying homogeneous g ani e
bed ock a an a e age o 0.6m dep h. The s udy a ea is de-
ined as he a ea inside he bo de s o wo mini-ca chmen s
(C1, 889m2, and C2, 301m2) ha ecei e wa e only om
p ecipi a ion, since hey a e loca ed a he op o a small hill
(Fig. 1). The mini-ca chmen bo de s we e mapped based on
bed ock opog aphy, and measu ed by soil pene a ing ada
in 1994. Two conc e e wei s we e buil o guide he la e al
ou low o wa e o ou le s o he wo wei s. The ada mea-
su emen showed ha he e we e no majo e ical c acks in
he bed ock. The lowes soil laye on he bed ock has a high
sil ac ion, ende ing he wa e shed wa e igh . Thus wa e
lows in he soil along he di ec ion o he slope and ou low
occu s only ia he ou le s in he wei s as epo ed in Il es-
niemi e al. (2010).
2.2 Ni ogen pools
2.2.1 To al and non-soluble ni ogen in soil
The pool o N bound o he soil ma ix ( he non-soluble soil
N pool) was calcula ed by sub ac ing ex ac able and soil
wa e N pools om he o al soil N pool.
The o al soil N pool was de e mined om soil samples
collec ed om di e en soil ho izons in 1995. The samples
we e aken using s eel cylinde s (148cm3 olume, 6cm di-
ame e ) om each mo phologic soil ho izon (L/F/H, elu ial
E ho izon, illu ial B ho izon and pa en ma e ial C ho izon)
Biogeosciences, 10, 1083–1095, 2013 www.biogeosciences.ne /10/1083/2013/
J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es 1085
om he e ical ace o 5 soil pi s. The samples we e ai
d ied a 60◦C, sie ed h ough a 2mm sie e, and g ound be-
o e he analysis. The C and N con en s o each sample we e
analyzed using an elemen al CN analyze (LECO, Leco Co -
po a ion, S . Joseph, MI, USA).
The N pool was calcula ed o each soil ho izon and o
each pi by using a ho izon-speci ic a e age o each o he
ollowing: N concen a ion, ho izon dep h, soil densi y and
s one ac ion. The N pool o each soil ho izon was calcu-
la ed as he a e age o he N pools o he speci ic ho izon in
each pi . The o al soil N pool was calcula ed as he sum o
N pools o all ho izons.
2.2.2 Ex ac able ni ogen in soil
The ex ac able pools o soil ammonium (NH+
4-N), ni a e
(NO−
3-N) and o ganic ni ogen (No g)we e de e mined om
samples aken om li e - and humus-laye s and om min-
e al soil a 0–0.1m and 0.1–0.3m dep hs. The samples we e
collec ed wi h a Wes man soil auge (Wes man, 1995) 1 o
3 imes pe yea (8 imes in o al) om 2006 o 2009. F esh
soil samples we e ex ac ed wi h 2MKCl o 2h, and he
ex ac s we e il e ed h ough Wha man 40 il e pape s and
ozen un il analysis. Dissol ed NH+
4, NO−
3and No g in he
ex ac s we e analyzed by low-injec ion spec ome y, as de-
sc ibed in Sec . 2.3.2. Ni ogen pools on soil pa icle su aces
we e es ima ed by sub ac ing N pools in soil wa e in he up-
pe mos 0.3m dep h om he measu ed alues o ex ac able
N pools.
2.2.3 Ni ogen in soil wa e
The pools o NH+
4-N, NO−
3-N and No g in soil wa e we e
calcula ed by measu ing he concen a ions in e e y soil
laye , and mul iplying he measu ed concen a ions wi h soil
wa e s o age speci ic o each soil ho izon. Laye speci ic soil
wa e pool was calcula ed based on ime-domain e lec om-
e y measu emen s, as desc ibed in Il esniemi e al. (2010).
The concen a ions o NH+
4-N, NO−
3-N and No g we e mea-
su ed in soil wa e samples ob ained wi h suc ion cup lysime-
e s. Suc ion cups we e ins alled a 7 loca ions (pi s) and a
each loca ion in e e y soil ho izon. Samples we e collec ed
in weekly o o nigh ly in e als du ing he pe iods when he
soil was no ozen. A he ime o sampling, a suc ion pump
(−400mba ) was applied o he ubes connec ed wi h suc ion
cups in di e en soil dep hs. Wa e was sampled when ei he
he wa e olume eached a minimum o 250mL, o a e 7 o
34h o collec ing. Du ing he summe mon hs when he soil
was ela i ely d y, e en he 34-h collec ion did no p o ide
su icien amoun s o wa e om all loca ions. To de e mine
he a io be ween ni a e and ni i e (NO−
3:NO−
2)in soil wa-
e , we used da a measu ed in 1997. Ni a e (NO−
3)and ni i e
(NO−
2)concen a ions we e measu ed colo ime ically om
he d ainage low wa e by a ni a e educ ion ube wi h cad-
mium column (Do ich and Nelson, 1984). The wa e analysis
is explained in Sec . 2.3.2.
2.2.4 Abo eg ound biomass ni ogen
To es ima e N pools in abo eg ound biomass, he diame-
e a 1.3m heigh and heigh o e e y ee in he ca ch-
men we e measu ed. Reg ession unc ions desc ibed in Re-
pola (2008, 2009) we e used o model he d y weigh o
wood, s ems, ba k, needles, lea es, oo s, ali e b anches,
and dead b anches. The d y weigh s o he biomass classes
we e hen mul iplied wi h he ep esen a i e N concen a-
ions, p esen ed in Table 1. The da a o coni e ous needles
used in he eg ession we e collec ed in he au umn, when
pa o he needles we e al eady shed (Repola, 2009). The e-
o e he model gi es an unde es ima ion o he maximum o-
liage pool. As ollows, 60% o he annual needle li e all
was added o he es ima ion, as based on he li e all mea-
su emen s on he si e. This 60% ep esen s he amoun o
needle li e all occu ing du ing he au umn.
Annual biomass N pool change (1B; kgNha−1y −1)cal-
cula ions we e based on he di e ence be ween he biomass
classes om 2003 and 2008. We conside he model esul s
o he inc ease o wood and ba k biomass o be ela i ely
eliable, bu we conside he biomass change in b anches and
oliage o be only sugges i e, because he needle mass is usu-
ally assumed no o inc ease a e he canopy has been closed.
2.3 Ni ogen anspo in wa e
2.3.1 Sampling and main enance
Bulk deposi ion, h ough all and s em low wa e s we e col-
lec ed in canis e s, which we e changed mon hly du ing he
win e and once a o nigh du ing he summe , o when-
e e hey we e ge ing ull. All o he canis e s we e al-
ways changed a he same ime. The canis e s we e washed
wi h ho wa e and Deconex®labo a o y cleaning de e gen
(Bo e Chemie AG, Zuchwil, Swi ze land), insed wi h ap
wa e h ee imes, and inally insed wice wi h deionized wa-
e . Th ough all collec o s we e cleaned daily using a b ush,
deionized wa e , and washclo h o emo e needles, pollen
and o he di . No an i-mic obial subs ances we e used in he
canis e s o he h ough all collec o s. The wa e collec ing
sys em is desc ibed in mo e de ail by Il esniemi e al. (2010).
2.3.2 Labo a o y wa e analyses
The wa e samples (p ecipi a ion, h ough all, s em low, soil
wa e and d ainage low) we e analyzed as ollows: (1)
he amoun o collec ed wa e was measu ed by weigh-
ing (1kg≈1dm3), (2) p ecipi a ion, h ough all and s em-
low subsamples we e each pooled in o one sample (3)
pH and elec ic conduc i i y we e measu ed, (4) p ecipi a-
ion, h ough all, and s em low samples we e il e ed wi h
a acuum-d i en il e ing sys em (Millipo e) using 0.45µm
www.biogeosciences.ne /10/1083/2013/ Biogeosciences, 10, 1083–1095, 2013
1086 J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es
memb ane il e s (Millipo e), and (5) samples we e bo led
and s o ed a −17◦C un il u he analysis.
Ammonium (NH+
4), ni a e (NO−
3)and o ganic ni ogen
(N o )we e measu ed om all he wa e samples and he soil
ex ac s by low-injec ion spec ome y a he Finnish Fo es
Resea ch Ins i u e, Van aa Uni (modi ied ISO 11732:2005
(FIA), SFS-EN ISO 13395:1997: SFS-EN ISO 11905-
1:1998 (FIA), espec i ely). De ec ion limi s o NH+
4-N,
NO3-N, and N o we e 0.03, 0.001 and 0.1mgdm−3, espec-
i ely. O ganic N (No g)was de e mined using o al N con-
cen a ions in he samples as ollows:
[No g]=[N o ]−[NH+
4−N]−[NO−
3−N].(1)
The il e ing o he soil ex ac s wi h Wha man 40 il e pa-
pe (8µm) does no emo e all he pa icula e N. The e o e,
we ecognize ha he No g includes bo h dissol ed o ganic
ni ogen and some pa icula e N.
2.3.3 S em low
S em low was measu ed om 2006 o 2009 du ing snow- ee
pe iods om 4 ees by di ec ing s em low wa e in o insu-
la ed canis e s. Fo ha pu pose clea ed silicon ubbe ubes
(diame e 25mm) we e a ached a ound he ees. The N lux
a e in sepa a e chemical N o ms (NH+
4-N, NO−
3-N, No g)in
s em low (Sc; mg Nm−2day−1)in he o es was calcula ed
as ollows:
Sc=1
4X4
i=1
Ab o
Abi
Cci Vci
(AC1 +AC2) ,(2)
whe e “c” e e s o he chemical o ms o N, i e e s o a mea-
su ed ee, 4 is he numbe o measu ed ees, Cci is he con-
cen a ion o N (mgdm−3)in he s em low wa e in di e en
chemical o ms (NO−
3-N, NH+
4-N, No g),Vci is he olume
o he collec ed s em low wa e (dm3), Abiis he s em c oss
sec ion a ea o he ees om whe e he s em low was mea-
su ed, Ab o is he o al s em c oss sec ion a ea o he ees in
he ca chmen s (m2; C1+C2), AC1 and AC2 a e he a eas o
he wo mic o-ca chmen a eas (m2) desc ibed in Sec . 2.1,
and is he leng h o he collec ion pe iod (in days).
2.3.4 D ainage low
As desc ibed in Sec . 2.1, he s udy si e is de ined as he a ea
inside wo mic o-ca chmen s, and he ou low wa e is di-
ec ed o he wo wei s. The wa e low h ough he wei s was
measu ed au oma ically wi h a low me e (Schlumbe ge
Aqua ic, Schlumbe ge Wa e Se ices, Pa is, F ance), and
when low exis ed, wa e was sampled o chemical analysis
on a daily basis om he ou le o he wei s. The daily sum
o wa e low was mul iplied wi h he concen a ions o di -
e en chemical o ms o N (NH+
4-N, NO−
3-N, No g) o ge
he daily N luxes sepa a ely. When he concen a ions we e
unde he de ec ion limi , we used hal o he de ec ion limi
as he measu ed alue. We also calcula ed he lowe and he
uppe alues o he N lux in he d ainage low by assuming
ha he lowe alue was ze o and ha he uppe alue was he
de ec ion limi . The lowe and uppe alues we e used o cal-
cula e he unce ain y o he a e age lux. The d ainage low
measu emen s a e explained in mo e de ail in Il esniemi e
al. (2010).
2.4 A mosphe ic N deposi ion
The o al annual N deposi ion o he si e was calcula ed as
he sum o es ima ed we and d y deposi ion. We deposi ion
was es ima ed om he measu ed bulk deposi ion da a, and
he alues o d y deposi ion we e aken om Flecha d e
al. (2011).
2.4.1 Bulk deposi ion
Di e en N componen s (NO−
3, NH+
4, No g)in he bulk N
deposi ion we e sampled in a owe abo e he o es canopy
using wo ain wa e collec o s made o polye hylene un-
nels (0.13m2in a ea; Plas ex Oy, Lohja, Finland). In he
win e , snow all was collec ed in o ci cula canis e s (0.2m2
in a ea). The canis e s we e changed mon hly in win e and
once a o nigh in summe , o whene e hey we e ge ing
ull. No an i-mic obial subs ances we e used in he canis e s.
The bulk deposi ion a e was calcula ed by mul iplying mea-
su ed concen a ions o NO−
3, NH+
4and No g by p ecipi a-
ion and di iding by collec ion ime. The p ecipi a ion was
measu ed op ically wi h a DRD12 ain de ec o (Vaisala Oyj,
Helsinki, Finland). The wa e collec ing sys em is desc ibed
in mo e de ail by Il esniemi e al. (2010).
2.4.2 Th ough all
Th ough all wa e was collec ed using se en ec angula
ainwa e collec o s ins alled below he o es canopy a
app oxima ely 0.5m heigh om soil su ace. The collec-
o s we e made o s ainless s eel and we e 4m long and
0.1m wide, wi h e ec i e wa e collec ing a ea (A )be-
ing 0.385m2. Th ough all wa e s we e collec ed in insula ed
canis e s ins alled below he midpoin o each collec o . Du -
ing he win e , when p ecipi a ion was domina ed by snow-
all, he h ough all collec o s we e eplaced wi h ci cula
canis e s (0.2m2).
Th ough all a es (Tc; mgNm−2d−1)we e calcula ed as
ollows:
Tc=c cV
A ,(3)
whe e subsc ip “c” e e s o he concen a ion o N s o ed in
di e en chemical o ms (NO−
3, NH+
4o No g),c cis he con-
cen a ion o he compound in he wa e sample (mg dm−3),
V is he olume o he wa e sample (dm3),A is a ea o he
collec o , and is he leng h o he collec ion pe iod (days).
Biogeosciences, 10, 1083–1095, 2013 www.biogeosciences.ne /10/1083/2013/
J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es 1087
Fig. 1. Map o he measu emen si e indica ing he sampling design o measu ing ni ogen luxes in p ecipi a ion, h ough all, s em low,
li e all, d ainage low, NO- and N2O-emissions and ni ogen pools in he soil wa e . The wo ca chmen a eas (C1, C2) a e ma ked on he
map wi h a line, and he d ainage low is di ec ed o he wo wei s on op o he map. The heigh and he diame e a 1.3m o e e y ee in
he ca chmen a eas we e measu ed o biomass in en o y.
2.4.3 Es ima ing we deposi ion om bulk deposi ion
measu emen
The bulk deposi ion measu emen gi es an unde es ima ion
o he o al (we +d y) deposi ion, and an o e es ima ion o
he we deposi ion. This is due o he ac ha in he bulk
deposi ion measu emen , some bu no all o he d y deposi-
ion is included. A simple model o ac iona e he bulk de-
posi ion in o we and d y deposi ion was o mula ed based
on he amoun o p ecipi a ion and he pe iod o ime du ing
which he d y deposi ion could ha e occu ed. As he esul ,
he model gi es an es ima e o we nu ien deposi ion o he
ecosys em. The model also gi es an es ima ion o he d y de-
posi ion, bu only o he deposi ion on he bulk deposi ion
collec o , no he deposi ion o he whole ecosys em. As a e-
sul o he model, we ge ha he we deposi ion was 57% o
he measu ed bulk deposi ion. To calcula e he o al we de-
posi ion a he si e, he amoun o bulk deposi ion was mul i-
plied by his numbe (57%). The model is desc ibed b ie ly
in Ko honen e al. (2012).
2.4.4 D y deposi ion
The mean o he d y deposi ion o ou models p esen ed in
Flecha d e al. (2011) o Hyy i¨
al¨
a we e used as an es ima e
o he d y deposi ion. When his d y deposi ion da a was used
in conjunc ion wi h he measu ed bulk deposi ion da a om
his s udy, he modeled ae osol pa icle NH+
4and gaseous
NH+
3deposi ion we e coupled wi h he measu ed NH+
4depo-
si ion, and modeled ae osol pa icle NO−
3and gaseous NO2
and HNO3deposi ion we e coupled wi h he measu ed NO−
3
deposi ion.
2.5 Gaseous emissions
2.5.1 Ni ous oxide (N2O)
The luxes o ni ous oxide (N2O) we e measu ed wi h one
au oma ic and six manual s a ic chambe s. The au oma ic
chambe and ou o he manual chambe s we e loca ed
in he wo ca chmen a eas, whe eas wo manual chambe s
we e loca ed ou side he ca chmen (Fig. 1). The au oma ic
chambe was made o s ainless s eel (0.40×0.80×0.32m:
wid h×leng h×heigh ), and was equipped wi h wo ans
and a he mocouple o chambe ai empe a u e measu e-
men . The chambe was au oma ically closed 1–4 imes pe
day o 60min. Du ing each enclosu e a minimum o 4 gas
samples we e wi hd awn om he headspace by a cus om-
made au osample (MaSa, Pohja-Me alli y¨
opaja, Juupajoki,
Finland). The manual chambe s we e made o s ainless-s eel
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1088 J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es
Table 1. Ni ogen concen a ions o abo eg ound biomass classes
used o biomass ni ogen pool calcula ions. The wood concen a-
ion was measu ed in Juupajoki, nea he measu emen si e.
Biomass class N Desc ip ion Re e ence
(mgg−1)
Wood 0.72 Li e a u e M¨
alk¨
onen
(1974)
Sco s pine 12 Measu ed Palm o h and Ha i
needles on si e (2001)
No way sp uce 11 Li e a u e B aekke e al.
needles (1998)
B oad-lea ed 24 Li e a u e Be g and
species McClaughe y (2003)
Ba k 4.2 Measu ed Li e ap da a
on si e ( his s udy)
B anches 1.3 Measu ed Li e ap da a
on si e ( his s udy)
(0.29×0.40×0.24), and hey we e equipped wi h a an and
a sample po in he middle o he chambe (Pihla ie e al.,
2007).
The manual chambe measu emen s we e conduc ed on a
weekly basis du ing summe mon hs and mon hly in he win-
e as desc ibed by Pihla ie e al. (2007). The concen a ions
o N2O in he gas samples we e analyzed by a gas ch oma o-
g aph equipped wi h an elec on cap u e de ec o . N2O luxes
we ecalcula ed bylinea eg essionme hod. Non-linea i yo
he concen a ion change o e chambe closu es was es ed.
Due o measu ing N2O luxes close o he de ec ion limi (see
Pihla ie e al., 2007), we chose o use he linea eg ession
me hod as he mo e obus calcula ion me hod o he N2O
luxes.
2.5.2 Ni ogen oxide (NO)
Flux o NO om he soil was measu ed using h ee au o-
ma ic dynamic low- h ough chambe s du ing a sho cam-
paign om 15 July o 30 Oc obe 2011. The chambe -
sys em consis ed o h ee anspa en chambe s simila o
he au oma ic N2O chambe , and wi h luo ina ed e hylene–
p opylene ilm as he anspa en wall ma e ial. The ope -
a ion o he chambe s was au oma ed; each chambe was
closed o 15min once e e y h ee hou s. Sample ai was
d awn om he chambe s a a a e o 4.1dm3min−1in o
a chemiluminescence analyse (TEI 42S, The mo En i on-
men al Ins umen s, Philadelphia, PA, USA). The measu e-
men p inciple o he soil NO lux was simila o ha o he
shoo NOx lux desc ibed in Rai onen e al. (2003), excep
ha an emp y chambe was no used as a e e ence chambe .
A he ime o he sampling, compensa ion ai om he abo e
canopy a mosphe e was di ec ed in o he chambe s a a a e
o 4.5dm3min−1. Soil lux was calcula ed using a lux cal-
cula ion me hod o low h ough chambe s as desc ibed in
Kola i e al. (2012).
Table 2. Ni ogen and ca bon con en s and ca bon- o-ni ogen-
a ios in he annual li e all, and in di e en li e ac ions in Sco s
pine o es a Hyy i¨
al¨
a du ing 2006 o 2008. “Cones and seeds” ep-
esen s all he ma e ial dis inguished as ep oduc i e ma e ial, bu i
mos ly consis s o cones. Unce ain y is s anda d e o o he annual
means.
Cmgg−1Nmgg−1C:N
Needles 512±3 4.9±0.3 104±7
Lea es 486±4 8.8±0.7 55±5
La ge b anches 499±0 4.7±0.1 105±1
Small b anches 494±2 4.4±0.3 113±7
Ba k 492±6 3.7±0.2 134±6
Cones and seeds 471±3 2.1±0.2 221±18
O he 503±3 12±1 41±2
To al 502±3 5.1±0.3 99±6
2.6 In e nal cycling
2.6.1 Li e all
Li e all was measu ed mon hly om 2006 o 2010 using
20 ci cula li e collec o s (0.2m2each) ins alled sys ema -
ically on he wo ca chmen a eas (Fig. 1) as desc ibed in
Il esniemi e al. (2009). The li e collec o s we e emp ied
once a mon h, d ied a 60◦C o 24h, and weighed. D ied
li e was hen sepa a ed in o needles, lea es, ba k, b anches,
seeds (including cones), and emaining ma e ial. Each com-
pa men was weighed, g ound, and pooled. Ca bon and N
concen a ions we e measu ed om he pooled samples by
elemen al CN analyze ( a io Max CN, Elemen a Analy-
sensys eme GmbH, Hanau, Ge many). The N concen a ions
o li e ac ions a e p esen ed in Table 2. La ge b anch
li e was collec ed in o 20 ames (0.5×1.0m) lying on
he g ound. The b anches we e collec ed once a yea and
ea ed simila ly as he o he li e . The N lux in li e all
(L; gNm−2y −1)is
L=1
20
20
X
i=1
(mciCc)1
AL ,(4)
whe e i e e s o he numbe o he li e collec o s o he
b anch ames, “c” e e s o di e en biomass compa men s,
mci is he mass o collec ed li e compa men (g), Ccis N
concen a ion (mgNg−1),ALis he a ea o he collec o , and
is he leng h o collec ion pe iod (in days).
2.6.2 Ni ogen e ansloca ion and senescence
Based on Helmisaa i (1992), e ansloca ion o N (R;
kgNha−1y −1)was calcula ed as ollows:
R=1.49mbcg−mbcb
AL
,(5)
whe e mbis he mass o (b own) oliage li e collec ed by
li e aps pe yea (g), cbis he N concen a ion o ha li e
Biogeosciences, 10, 1083–1095, 2013 www.biogeosciences.ne /10/1083/2013/
J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es 1089
(mgg−1),cgis N concen a ion o g een needles (12mgg−1;
Palm o h and Ha i, 2001), ALis he a ea o he li e collec-
o , is he li e collec ion ime (1y ), 1.49 is he ela i e
mass o a single g een needle o a single b own needle, cal-
cula ed as an a e age om he h ee plo s om a ious yea s
(n=11) p esen ed by Helmisaa i (1992). This numbe was
applied o all ee species.
Plan N loss du ing senescence (S; kgNha−1y −1)was
calcula ed as he sum o li e all and e ansloca ion. Fo all
biomass classes o he han oliage, e ansloca ion was as-
sumed o be negligible. We assumed ha he pool o dead
plan ma e ial a ached o he ees does no change, and hus
ha he alues o N loss in he li e all ep esen he N loss
in senescence.
2.7 Va iables based on mass balance calcula ions
The o al N balance o he ecosys em (1Ns+1Nb;
kgNha−1y −1)was calcula ed as ollows:
1Ns+1Nb=Dw+Dd−EN2O−ENO−D ,(6)
whe e 1Nsis he change o N pools in he soil, 1Nbis he
change o N pool in abo eg ound biomass, Dwis he we N
deposi ion, Ddis he d y N deposi ion, EN2Oand ENO a e
he N losses in N2O and NO emissions, espec i ely, and D
is N loss in he d ainage low.
The amoun o N used o g ow h (Yi; kgNha−1y −1)was
calcula ed as ollows:
Yi=1Bi+Si,(7)
whe e 1Biis he change o N in biomass and Siis he senes-
cence in he biomass class, bo h measu ed in kgNha−1y −1
and whe e subsc ip i e e s o he abo eg ound biomass
class (needles, lea es, b anches, ba k, wood). The o al
amoun o N used by plan s (B o ; kgNha−1y −1)was calcu-
la ed as he sum o N used o each indi idual abo eg ound
biomass class.
Ni ogen up ake by plan s (U; kgNha−1y −1)was calcu-
la ed as ollows:
U=B o −R, (8)
whe e B o is N use by plan s and Ris he e ansloca ion o
N.Ne elease o N om he decomposi ion
(Rd;kgNha−1y −1)was calcula ed by assuming ha
he pool o plan -a ailable-N is cons an in a ime scale o a
couple o yea s as ollows:
Rd=U+E o +D −D o ,(9)
whe e Uis N up ake by plan s, E o is he gas emission o N
(EN2O+ENO),D is he d ainage low and D o is he o al
deposi ion (Dw+Dd), all in kgNha−1y −1.
Table 3. Ni ogen concen a ions, ni ogen pools and ca bon- o-
ni ogen a ios in di e en physical soil ho izons (O, A, B, C1 and
C2). The a e age dep h o he mine al soil is 0.59m.
O A B C1 C2
Ho izon hickness (m) 0.05 0.041 0.16 0.19 0.20
N concen a ion (mgg−1)13 1.2 1.0 0.17 0.053
N pool (kgNha−1)* 710 240 860 190 75
C:N 28 33 23 36 19
* 1ha=10000m2.
The change o he non-soluble soil N pool (1Nsom;
kgNha−1y −1)was calcula ed as ollows:
1Nsom=L−Rd,(10)
whe e Lis N lux in he li e all and Rdis he ne elease o
N om he decomposi ion, bo h in kgNha−1y −1.
3 Resul s
3.1 Soil ni ogen pools
The o al N pool in he soil was 2070kgNha−1
(1ha−1=10000m−2). The as majo i y o he soil N was
bound o he soil ma ix (2050kgNha−1). The o ganic laye
(li e and humus) and he uppe mos 0.2m mine al soil ho i-
zons (A and B ho izons) con ained 710 and 1100kgNha−1,
espec i ely, which comp ised 87% o he o al soil N (Ta-
ble 3). The highes N concen a ion in he soil was in he
o ganic laye , 12.9mgg−1o soil. In he mine al soil he
N concen a ion was on he o de o 1mgg−1in he A
and B ho izons, and on he o de o 0.1mgg−1, in he C1
and C2 ho izons. The calcula ed soil non-soluble N accu-
mula ion a e (1Nsom)was −1kgNha−1y −1, sugges ing a
sligh dec ease in he soil N pool. Howe e , he es ima ion
does no di e om 0, aking in o accoun he e o ma gin
(±8kgNha−1y −1).
The ex ac able N pool in he o ganic laye and he op-
mos 0.30m o he mine al soil (26.8kgNha−1)was small
compa ed o he o al soil N pool. O he ex ac able soil N al-
mos all (98.9%) was in o ganic o m (No g), 26.5kgNha−1.
The as majo i y o he mine al N was ammonium-N (NH+
4-
N; 0.31kgNha−1; 99.4%), and only a mino ac ion was
ni a e-N (NO−
3-N; 2gNha−1; 0.6%). The ni a e-N es ima-
ion is ela i ely unce ain.
N pool in soil wa e was 0.70kgNha−1, and simila o
he ex ac able N, he majo i y o i was in o ganic o m
(0.66kgNha−1). Ammonia and NO−
3pools in he soil wa-
e we e app oxima ely 30 and 3g Nha−1, espec i ely. Ni-
a e concen a ions we e ypically unde he de ec ion limi ,
and hus he ex ac able and especially soil wa e NO−
3pool
sizes a e unce ain. A mo e eliable es ima ion was ob ained
om he ex ac ed NO−
3concen a ion, which includes bo h
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1090 J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es
Table 4. The measu ed a mosphe ic annual bulk N deposi ion, es i-
ma ed annual we N deposi ion and modeled annual d y N deposi-
ion, all in kgNha−1y −1).
NH+
4NO−
3No g To al
Measu ed bulk deposi ion 1.3 2.1 1.5 4.9
Es ima ed we deposi ion 0.7 1.2 0.9 2.8
Modeled/es ima ed d y deposi ion 1.0* 2.5* 1.1 4.6
Es ima ed o al deposi ion 1.7 3.7 2 7.4
Measu ed h ough all 0.5 1.1 1.4 3.0
* Flecha d e al. (2011); NH+
4and NH3a e combined as NH+
4, and NO−
3, NO2and
HNO3a e combined as NO−
3. O ganic N deposi ion was no included in he s udy.
NO−
3-N in soil pa icle su aces and in soil wa e . Based on
he measu emen s in 1997, he median and mean a ios be-
ween ni a e and ni i e (NO−
3:NO−
2)in he d ainage wa e
measu emen s we e 9.3 and 7.4, espec i ely.
3.2 Biomass ni ogen pools
Ni ogen s o ed in he abo eg ound ee biomass in 2008
was 210kgNha−1, which was 9% o he o al N in
he ecosys em. Ni ogen was dis ibu ed qui e e enly
o oliage (77kgNha−1), b anches (58kgNha−1), wood
(49kgNha−1)and ba k (24kgNha−1). O he b anch N
pool, 12kgNha−1was es ima ed o be s o ed in dead
b anches.
The o al N accumula ion o abo eg ound biomass was
7.4kgNha−1y −1. The wood and ba k biomass inc ease
we e 2.3 and 0.8kgNha−1y −1, espec i ely. The mo e un-
ce ain es ima es o oliage and b anch biomass accumula-
ion we e 1.8 and 2.6kgNha−1y −1, espec i ely.
3.3 A mosphe ic N deposi ion and h ough all
Mos o he o al a mosphe ic deposi ion
(7.4kgNha−1y −1)occu ed in he o m o d y depo-
si ion (4.6kgNha−1y −1). Mos o he o al deposi ion was
in mine al o m, bu o ganic deposi ion con ibu ed o e
one ou h o he o al deposi ion. Be ween 2006 and 2010
he annual measu ed bulk N deposi ion a ied om 4.0
o 6.3kgNha−1y −1, he mean bulk N deposi ion being
4.9kgNha−1y −1. The dis ibu ion o he deposi ion is
desc ibed in Table 4.
The measu ed h ough all o N was 2.9kgNha−1y −1,
which consis ed mos ly o No g and NO−
3-N, 1.4 and
1.1kgNha−1y −1, espec i ely. The measu ed N lux in
s em low, 0.1kgNha−1y −1, was e y low compa ed o
h ough all, and consis ed mainly o No g. The measu ed con-
cen a ions o NH+
4and NO−
3we e 25% o 90% highe in
bulk deposi ion han in h ough all, bu he concen a ion o
No g was on a e age 33% highe in h ough all han in bulk
deposi ion. Howe e , he measu ed h ough all lux was on
a e age lowe han he measu ed bulk deposi ion o mine al
N and No g.
3.4 D ainage low and gaseous emissions
Annual N lux om he ecosys em ia d ainage low a -
ied be ween 0.04 and 0.23kgNha−1y −1and was on a -
e age 0.13kgNha−1y −1. The N lux in d ainage low was
domina ed by No g, on a e age 0.12kgNha−1y −1. The a -
e age lux o mine al N in d ainage low was e y low,
0.005kgNha−1y −1and 0.002kgNha−1y −1 o NH+
4and
NO−
3, espec i ely. The unce ain y o he mine al N alues
is app oxima ely ±50%, and o he o ganic N up o ±90%.
The unce ain y is p ima ily caused by he ac ha he luxes
we e e y small and mos o he ime he N concen a ions
we e below he de ec ion limi . The e o e, i is mo e likely
ha ou es ima e o he d ainage low is an o e es ima ion
han an unde es ima ion.
Bo h N2O and NO we e emi ed om he soil and NO2
was deposi ed in o he soil, howe e , he luxes we e e y
small. Annual cumula i e soil N2O emission a e aged o
0.2kgNha−1y −1. Measu ing NO emission and NO2depo-
si ion om/ o he soil was challenging because o he small
luxes. Du ing he campaign in he au umn pe iod 2011, mea-
su ed NO-N emission was a ound 0.01kgNha−1y −1and
NO2-N deposi ion was e en smalle .
3.5 Ni ogen balance
The inpu s o he sys em we e one o de o magni ude highe
han he ou pu s (Fig. 2). The o al N accumula ion was
7kgNha−1y −1. D y deposi ion was highe han we depo-
si ion, bu hey bo h we e on he same o de o magni ude.
App oxima ely h ee ou hs o he N los om he sys em
was in he o m o gaseous N2O-N emissions, and one hi d
as No g in he d ainage low. Ni ous oxide (N2O) emission
o N deposi ion a io was app oxima ely 0.03 and N2O:NO
emission a io was app oxima ely 20.
3.6 In e nal ni ogen cycling
3.6.1 Li e all
F om 2006 o 2010, he amoun o N lux in annual
abo eg ound li e all om ees a ied om 14 o
22kgNha−1y −1, being on a e age 18kgNha−1y −1. Hal
o he N lux in he abo eg ound li e all was in needles and
lea es, 8.0 and 1.0kgNha−1y −1, espec i ely. B anches
con ibu ed abou one ou h o he N in abo eg ound li -
e all, 5.3kgNha−1y −1. Ni ogen lux in he li e all o
ba k, ep oduc i e ma e and uniden i ied ma e we e 1.1,
0.35 and 2.1 kgNha−1y −1, espec i ely.
3.6.2 Senescence and e ansloca ion
Ni ogen e ansloca ion om needles and lea es was es i-
ma ed o be 21kgNha−1y −1and 2.8kgNha−1y −1, e-
spec i ely. This was 73% o he ini ial amoun o N in he
Biogeosciences, 10, 1083–1095, 2013 www.biogeosciences.ne /10/1083/2013/
J. F. J. Ko honen e al.: Ni ogen balance o a bo eal Sco s pine o es 1091
Fig. 2. Inpu s (A) and ou pu s (B) o N in bo eal Sco s pine o es in Hyy i¨
al¨
a. No e he di e en y-scale in he images. The e o ba o
he we deposi ion is based s anda d e o o mean o he annual p ecipi a ion amoun and on he unce ain y o es ima ing N concen a ion
in p ecipi a ion om bulk deposi ion measu emen . The e o ba o he d y deposi ion ep esen s he s anda d de ia ion be ween he ou
models used in Flecha d e al. (2011) and he unce ain y o es ima ing No g. Sys ema ic unce ain y in he models and unce ain y in he
model inpu pa ame e s a e no included. The e o ba o he gas emission is he s anda d e o o mean o a e age lux be ween he chambe s.
The e o ba o he d ainage low is he s anda d e o o mean annual d ainage low o yea s 2006–2010.
oliage. Ni ogen e ansloca ion was highe han he N lux
in he abo eg ound li e all.
Ni ogen lux in li e all o b anches, ba k, cones and
uniden i ied li e was assumed o p esen he N loss in senes-
cence. The senescence o needles and lea es was es ima ed o
be 33 and 3.9kgNha−1y −1, espec i ely. The o al senes-
cence was 43kgNha−1y −1, which is app oxima ely one
i h o he abo eg ound biomass N pool (210kgNha−1).
3.6.3 N use by plan s
Es ima ed N use o g ow h was 50kgNha−1y −1(Fig. 3).
Ni ogen up ake and e ansloca ion we e as impo an
sou ces o he N use, 26 and 24kgNha−1y −1, espec i ely.
Ni ogen up ake comp ised 19 and 7kgNha−1y −1o ne N
elease om decomposi ion and deposi ion, espec i ely.
Mos o he used N, 36kgNha−1y −1, was alloca ed o
he oliage. The amoun o N used o g ow b anches, wood
and ba k we e 7.8, 2.3 and 1.9kgNha−1y −1, espec i ely.
The amoun o N used o g ow cones, seeds and lowe s
was ela i ely low, 0.35kgNha−1y −1. A ela i ely la ge
amoun , 2.1kgha−1y −1, o uniden i ied li e all was mea-
su ed. An equi alen amoun was in e p e ed o be used by
ees o g ow an unknown biomass ac ion.
4 Discussion
4.1 Ni ogen balance and in e nal ni ogen cycling
O e all N cycling a Hyy i¨
al¨
a Sco s pine o es is p esen ed in
Fig. 4. The ou pu s o N om he sys em a e e y small, and
N is accumula ing o he sys em a a a e o 7kgNha−1y −1.
In e nal cycling o N wi hin he o es is a e y impo an
sou ce o N o he plan s in his N limi ed ecosys em. Ni-
ogen e ansloca ion and N up ake a e equally impo an N
sou ces. Mos o he assimila ed N o igina es om he de-
composi ion o o ganic ma e . The a mosphe ic N deposi-
ion was abou one hi d o he o al N up ake. This means
ha elease du ing decomposi ion is he main o igin o N o
he plan up ake, bu also ha N deposi ion has clea ly in-
c eased he o al N up ake, boos ing he plan g ow h and
p oduc i i y. In e nal cycling and pools o N a Hyy i¨
al¨
a
we e sys ema ically sligh ly highe han hose o a simila
35-y -old Sco s pine o es in Mek ij¨
a i, sou heas Finland
(Helmisaa i, 1995). O e all, he esul s o hese s udies ag ee
e y well.
The amoun o N eleased om decomposi ion annually
is app oxima ely he same as he amoun o N eleased o
he soil in li e all. We hypo hesize ha a conside able pa
o he N eleased in decomposi ion o igina es om esh li -
e , which na u ally con ains mo e easily decomposable ac-
ions han old li e does. The e o e, we conclude ha he N
elease in he decomposi ion is a leas pa ly dependen on
he amoun o li e all. As he a mosphe ic N deposi ion
inc eases he plan g ow h, and hus also he li e all, we
a gue u he ha his e ec accumula es o e ime. The e-
o e, based on he N balance, he N deposi ion inc eases
plan p oduc i i y in h ee ways: (1) i di ec ly inc eases he
a ailabili y o plan -a ailable N, (2) i indi ec ly inc eases
he a ailabili y o N by inc easing he a e o e ansloca-
ion and he elease o N om he decomposi ion, and (3)
he indi ec e ec accumula es o e ime. In addi ion, i has
long been known ha N a ailabili y a ec s he lea - o- ine-
oo a io (Helmisaa i e al., 2007; E icsson, 1995), as hy-
po hesized in he unc ional balance concep (B ouwe , 1962;
Da idson, 1969). A low lea - o- ine- oo a io educes plan
g ow h, because o he ac ha when mo e ca bon is allo-
ca ed o he oo sys em, less ca bon is a ailable o he o-
liage g ow h. The la ge main enance cos s o a la ge oo sys-
em can be educed by highe N a ailabili y, and successi ely
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