ORIGINAL RESEARCH ARTICLE
published: 13 June 2014
doi: 10.3389/ pls.2014.00264
Fluo escence measu emen s show s onge cold inhibi ion
o pho osyn he ic ligh eac ions in Sco s pine compa ed
o No way sp uce as well as du ing sp ing compa ed o
au umn
Tapio Linkosalo*, Juha Heikkinen , Pe i Pulkkinen and Raisa Mäkipää
Van aa Uni , Finnish Fo es Resea ch Ins i u e, Van aa, Finland
Edi ed by:
Ka en Tanino, Uni e si y o
Saska chewan, Canada
Re iewed by:
Ge ha d Zo z, Ca l on Ossie zky
Uni e si ä Oldenbu g, Ge many
Ka en Tanino, Uni e si y o
Saska chewan, Canada
Flo ian A. Busch, The Aus alian
Na ional Uni e si y, Aus alia
*Co espondence:
Tapio Linkosalo, Finnish Fo es
Resea ch Ins i u e, PO Box 18,
Jokiniemenkuja 1, Van aa 01300,
Finland
e-mail: [email p o ec ed]
We s udied he pho osyn he ic ac i i y o Sco s pine (Pinus syl es is L.) and No way
sp uce (Picea abies [L.] Ka s ) in ela ion o ai empe a u e changes om Ma ch 2013
o Feb ua y 2014. We measu ed he chlo ophyll luo escence o app oxima ely 50 ees
o each species g owing in sou he n Finland. Fluo escence was measu ed 1–3 imes
pe week. We began by measu ing shoo s p esen in la e win e (i.e., Ma ch 2013)
be o e including new shoo s once hey s a ed o elonga e in sp ing. By July, when he
sp ing shoo s had achie ed simila luo escence le els o he olde ones, we p oceeded
o measu e he new shoo s only. We analyzed he da a by i ing a sigmoidal model
con aining ou pa ame e s o link sliding a e ages o empe a u e and luo escence. A
pa ame e de ining he empe a u e ange o e which p edic ed luo escence inc eased
mos apidly was he mos in o ma i e wi h in desc ibing empe a u e dependence o
luo escence. The model gene a ed simila luo escence pa e ns o bo h species, bu
di e ences we e obse ed o c i ical empe a u e and needle age. Down egula ion o
he ligh eac ion was s onge in sp ing han in au umn. Pine showed mo e conse a i e
con ol o he pho osyn he ic ligh eac ions, which we e ac i a ed la e in sp ing and mo e
eadily a enua ed in au umn. Unde he assump ion o a close co ela ion o luo escence
and pho osyn hesis, sp uce should he e o e bene i mo e han pine om he inc eased
pho osyn he ic po en ial du ing wa me sp ings, bu be mo e likely o su e os damage
wi h a sudden cooling ollowing a wa m pe iod. The win e o 2013–2014 was unusually
mild and simila o u u e condi ions p edic ed by global clima e models. Du ing he mild
win e , he ac i i y o pho osyn he ic ligh eac ions o bo h coni e s, especially sp uce,
emained high. Because ligh le els du ing win e a e oo low o pho osyn hesis, his
ac i i y may ansla e o a ne ca bon loss due o espi a ion.
Keywo ds: Sco s pine, No way sp uce, pho osyn hesis, phenology, cold inhibi ion, clima e change, os ole ance
INTRODUCTION
T ees g owing in he bo eal zone mus espond o a wide ange
o clima ic condi ions du ing a ypical yea . Fo e e g eens, his
means ha pho osyn he ic o gans mus be ac i e in he sum-
me bu become do man and os - esis an o he win e
(Leinonen and Hänninen, 2002). Sp ing is a demanding ime o
bo eal coni e s when ligh is abundan bu cold ai empe a u es
and possibly lack o a ailable wa e can hinde pho osyn hesis
(Suni e al., 2003). T ees a e locally adap ed o p e ailing con-
di ions, bu global wa ming will change he synch oniza ion o
empe a u e and ligh egime a a gi en loca ion, i.e., al hough
empe a u es a e expec ed o be highe , inciden adia ion will
emain he same. Inc easing empe a u es will a ec espi a-
ion du ing au umn and win e (Vesala e al., 2010) and pos-
sibly enhance pho osyn he ic ac i i y du ing sp ing (Hall e al.,
2009). The e o e, clima e change will impac he p oduc i i y o
bo eal o es s (Wang e al., 2011), bu he na u e o ha impac
will depend on how ees adap o he new empe a u e-ligh
egime (TLR).
The pho osyn he ic pa hway in coni e ous ees is ypical and
consis s o wo pa s; a ligh eac ion cap u es pho ons and s o es
hei ene gy in sho -li ed compounds be o e a da k (i.e., ligh
independen ) eac ion con e s hem in o mo e s able p oduc s.
The e iciency o he ligh eac ion is la gely de e mined by inci-
den adia ion while he da k eac ion is a complex biochemical
p ocess mo e dependen on p e ailing empe a u es (Po ca -
Cas ell e al., 2008). Consequen ly, a cold bu b igh TLR could
lead o unchecked ligh eac ions p oducing ee adicals ha
damage plan issues (Hune e al., 1998; Po ca -Cas ell e al.,
2008). In esponse o his p oblem, bo eal e e g eens can ac i ely
downg ade ligh eac ions aking place in hei pho osyn he ic
issues (Kola i e al., 2007).
As expec ed o locally-adap ed species, he po en ial pho o-
syn hesis o e e g eens ollows local changes in he TLR (O ande
www. on ie sin.o g June 2014 | Volume 5 | A icle 264 |1
Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
and Öquis , 1991; Beck e al., 2004). Due o he asynch ony
o empe a u e and ligh , he phenology o a gi en species will
a ec i s pho osyn hesis, g ow h, ep oduc ion, and isk o os
damage in al e ed clima es o he u u e. De elopmen o he
pho osyn he ic capaci y o bo eal coni e species has been ex en-
si ely s udied (Be gh e al., 1998; Lundma k e al., 1998; Leinonen
and Hänninen, 2002; Mäkelä e al., 2004; Kola i e al., 2007),
bu compa a i e s udies wi h di e en species in he same en i-
onmen al condi ions a e limi ed (Lundma k e al., 1988; Ög en
e al., 1997). Clea ly, i coni e s show species-speci ic esponses
o a gi en change in TLR, consequen changes o he p oduc-
i i y o bo eal o es s in he u u e will be de e mined by he
co-dis ibu ion o species and he new clima e. Compa a i e anal-
yses o species li ing in simila condi ions and modeling he da a
app op ia ely would imp o e he p ecision wi h which impac s
o clima e change on p oduc i i y and ecosys em heal h can be
p edic ed. Howe e , obse a ion pe iods mus include a wide
ange o clima ic condi ions in o de o de ec and in es iga e any
di e ences among species.
The goal o his s udy was o unde s and he ligh eac ion
dynamics o No way sp uce and Sco s pine in esponse o em-
pe a u e a ia iondu ing heyea .Wealsocompa edchlo ophyll
luo escence be ween sp ing and au umn. We hypo hesized ha
in compa ison o Sco s pine, pho osyn he ic ligh eac ions in
No way sp uce esume ea lie in sp ing and emain a highe
le els o mos o he win e . We i ed nonlinea mixed-e ec
models o ligh eac ion ac i i y based on a e age and minimum
daily empe a u es, and compa ed he p edic ions o sp uce and
pine in ela ion o changes in TLR.
MATERIALS AND METHODS
We measu ed he de elopmen o luo escence in 51 No way
sp uce (Picea abies [L.] Ka s ) and 48 Sco s pine (Pinus syl es is
L.) loca ed in he Haapas ensy jä common ga den (Finnish Fo es
Resea ch Ins i u e) in sou he n Finland (60◦37,24
◦25, 1250
d.d.). Mos sample ees o igina e om Finland (60–70◦N) bu
someo hesp uce eescame ompopula ionsincen alEu ope
(Table 1). No way sp uce a e g owing in a s and plan ed in
1980 and we e app oxima ely 15 m all when measu emen s we e
aken. Fo p ac ical easons, da a we e collec ed om shoo s ha
we e on he ou e edges o he sp uce s and whe e ees had
heal hy shoo s a leas down o b eas -heigh le el. We assumed
his o be an indica ion ha hese shoo s ecei ed su icien ligh
o main ain good condi ion.
The Sco s pine we e g a ed om shoo s collec ed om ma u e
ees in sp ing 2006 o oo s ocks sown a yea be o e. The g a s
we e plan ed in an open ield adjacen o he sp uce s and in 2007.
In 2013, he ees we e abou 1.5–2.0 m all; da a we e collec ed
om heuppe b anches.AllSco spineo igina ed omno he n
Finland (Table 1).
Fluo escence measu emen s began 06 Ma ch 2013 and con-
inued un il he end o Feb ua y 2014. Measu emen s we e
gene ally made weekly, inc easing o 2–3 imes a week when
ab up wea he changes and consecu i e changes in he luo es-
cen ac i i y o he ees we e expec ed. Measu emen s began wi h
needles o med du ing 2012 (he ea e e e ed o as 2012 nee-
dles), and we e la e expanded o include needles ha o med
Table 1 | O igin and numbe o ees s udied in his expe imen .
O igin Numbe o ees La i ude, ◦N
No way sp uce
(Picea abies [L.] Ka s )
Swi ze land 1 46.8
Czechoslo akia 4 48.9
Poland 2 51.4
Loppi, Finland 4 60.7
Längelmäki, Finland 5 61.6
Muu ame, Finland 6 61.9
Nu mes, Finland 5 63.5
Puolanka, Finland 5 64.9
Simo, Finland 11 65.7
Yli o nio, Finland 4 66.3
Sodankylä, Finland 2 67.4
Muonio, Finland 2 68.0
To al 51 −
Sco s pine
(Pinus syl es is L.)
I alo, Finland 13 68.6
Ke o, Finland 12 69.8
Ro aniemi, Finland 11 66.4
Sodankylä, Finland 12 67.3
To al 48 −
in he ea ly summe o 2013 (he ea e 2013 needles), once hey
had bu s ed. Bo h 2012 and 2013 needles we e measu ed in pa -
allel un il hei luo escence was he same in ea ly July, a e
which only 2013 needles we e measu ed. Measu ing needles o
di e en ages enabled he de elopmen o luo escence be ween
sp ing (i.e., 2012 needles) and au umn (i.e., 2013 needles) o be
obse ed. Fluo escence was measu ed in he ield wi h a hand-
held Pocke PEA luo ime e (Hansa ech, L d.), whe e needles
we e i s enclosed in ligh -p oo clips o a leas 30 mins o allow
all pho osyn he ic eac ions ime o comple e. The luo ime e
was hen a ached o he clip and a s ong pulse o ligh was passed
h ough he sample. Ini ially, mos o he ligh ene gy is abso bed
and p ocessed by he da k eac ion and he luo escen i a-
diance is a i s lowes alue (Fo). Sho ly he ea e he da k
eac ion becomes sa u a ed and su plus ene gy om he ligh
eac ion causes he luo escen i adiance o each a peak alue
(Fm). The luo ime e eco ds he ini ial and sa u a ed luo escen
i adiance and calcula es a ela i e index as:
Fm−FO
Fm
=F
Fm
(1)
The exp ession F /Fm e lec s he pho osyn he ic po en ial: when
ligh eac ions a e suspended, he e is minimal change in he lu-
o escen i adiance and, he e o e, alues a e small, while high
alues indica e ha he pho osyn he ic appa a us is ac i e.
Lea clips o he Pocke PEA luo ime e a e in ended o mea-
su e b oadlea species wi h la lea es. We modi ied he clips
o ensu e a ligh -p oo closu e o he clip a ound he cylin-
d ical sample needles (Figu e 1). Fo each ee, one shoo was
selec ed and agged o measu emen . Typically, wo needles we e
inse ed in o he ape u e o he clip. In epea ed measu emen s,
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Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
placemen o he clip on he shoo was selec ed andomly and
independen ly o ea lie samples.
Th oughou he measu ing pe iod, ou doo empe a u es we e
eco ded wi h a NTC- ype he mis o loca ed in a wea he -logge
boxinanopen ieldabou 200m om hes ands.Tempe a u e
was measu ed once pe minu e. Daily a e age empe a u e was
calcula ed as he a i hme ic a e age o all daily measu emen s,
FIGURE 1 | Clips used o measu e chlo ophyll luo escence modi ied
wi h an ex a oam pad added o he lowe jaw and a small ubbe
band o d aw he clip closed. These modi ica ions helped p o ide a
ligh -p oo closu e o he clip a ound he needles o be measu ed.
and daily minimum empe a u e was p oduced by selec ing he
minimum alue o each day (Figu e 2). To accoun o he ime
lag in he eac ion o ees o changing condi ions, we calcu-
la ed a mo ing a e age o he empe a u e using a ange o ime
cons an s om 1 o 12 days based on alues epo ed in he
li e a u e (see discussion). Fo compa ison (Figu e 2), we calcu-
la ed a long- e m daily a e age o 1961–2012 om empe a u e
measu emen s p o ided by he Finnish Me eo ological Ins i u e
(Venäläinen e al., 2005).
The dependence o luo escence measu emen s (pho osyn-
he ic ac i i y) on empe a u e was desc ibed wi h a non-linea
mixed e ec s model based on a ou -pa ame e logis ic esponse
unc ion:
F=amin +amax −amin
1+expT−c
b,(2)
whe e Fis he p edic ed luo escence, Tis he sliding a e age
o ei he he daily a e age o daily minimum empe a u e,amin
and amax a e he minimum and maximum asymp o es, espec-
i ely, bis a scale pa ame e de e mining he a e o ascen (i.e.,
alowe alueo b ansla es o a s eepe a e o ascen ), and c
is he empe a u e a which Fis hal way be ween amin and amax.
This empe a u e alue also co esponds o he la ges change o
luo escence ac i i y. Va iable cis e e ed o as he c osso e em-
pe a u e, in e p e ed as he empe a u e alue cha ac e izing he
c i ical empe a u e ange o pho osyn he ic ligh eac ions. The
asymp o ic alues amin and amax we e i edas ixedpa ame e s
FIGURE 2 | A e age ( ed line) and minimum (blue line) daily
empe a u es du ing he s udy pe iod. S onge colo s indica e
he pe iod o luo escence measu emen s, wi h 2 mon hs
p eceding he pe iod p esen ed in shaded colo s. The hinne ed
and blue lines show he long- e m mean and minimum daily
empe a u es ( ed and blue, espec i ely) om he Finnish
Me eo ological Ins i u e wea he da a om he yea s 1961 o 2012
(Venäläinen e al., 2005).
www. on ie sin.o g June 2014 | Volume 5 | A icle 264 |3
Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
sepa a ely o each species. The o he wo pa ame e s, band c,
we e i ed sepa a ely o each species as well as o he se o
obse a ions ep esen ing sp ing and au umn (i.e., 2012 and 2013
needles). Fu he mo e, band cwe e allowed o a y be ween ees
so ha he alue o b o he i h obse a ion is as ollows:
bi=bs(i),y(i)+βi,(3)
whe e s(i) and y(i) indica e he species and needle coho , espec-
i ely, and βiis a ze o-mean ee-speci ic andom e ec ; ciwas
modeled in a simila ashion. Va iances o he andom e ec we e
es ima ed sepa a ely o each species, bu a common es ima e o
esidual a iance was app op ia e. Based on he la e assump ion,
bo h species could be included in he same model, allowing o
he s a is ical es ing o di e ences be ween hem. Model i ing
was ca ied ou in he R-en i onmen (R Co e Team, 2013)wi h
he nlme package (Pinhei o e al., 2013), which uses app oxima e
maximum likelihood (Linds om and Ba es, 1990). Fo No way
sp uce, associa ion be ween ee o igin and c oss-o e empe -
a u e was assessed wi h Spea man’s ank co ela ion (Bes and
Robe s, 1975) o la i ude o o igin and es ima ed ee-speci ic
andom e ec in ci.
RESULTS
Fluo escence alues (Figu e 3) showed ha in sp ing 2013 he
ac i i y o he pho osyn he ic ligh eac ions in No way sp uce
s a ed o de elop ea lie , (i.e., a lowe ai empe a u es) han
in Sco s pine. Fluo escence in Sco s pine was lowe han ha o
sp uce h oughou he 6-week pe iod o de elopmen o pho o-
syn hesis in he sp ing. Bo h pine eached he same luo escence
le el as sp uce by he end o May.
Du ing he au umn, Sco s pine began a enua ing ligh eac-
ions ea lie and o lowe le els compa ed o No way sp uce,
bu as long as au umn empe a u es emained mild, luo es-
cence ac i i y did no each he lowes le els obse ed in he
p e ious sp ing. The win e o 2013–2014 was unusually mild in
sou he n Finland, wi h only mildly eezing empe a u es excep
o a cold pe iod o 3 days in ea ly Decembe and ano he
o 2 weeks in la e Janua y (Figu e 1). Du ing he i s cold
spell, pine luo escence dec eased o a much lowe le el han
sp uce. In bo h species, he pho osyn he ic appa a us was eac-
i a eda e hecoldspell,bu pine esumeda alowe le el
han sp uce. The cold pe iod in Janua y 2014 caused pine lu-
o escence o dec ease o a simila le el o he lowes obse ed
in ea ly sp ing 2013, while sp uce pe sis ed a a highe le el.
Ligh eac ions o bo h species eac i a ed when ai empe a u es
wa med, bu pine esumed ac i i y a a lowe le el compa ed o
sp uce.
A ange o ime cons an alues o he mo ing a e age o
empe a u e was es ed, and alues we e compa ed by i ing he
mixed model o each empe a u e eco d. The log-likelihood al-
ues o he model o each alue o he ime cons an a e gi en
in Table 2. A ime cons an alue o 7 days ga e he la ges log-
likelihood, bu di e ences among adjacen alues we e small.
Also, daily mean o daily minimum empe a u e only had a sligh
e ec on i o he mixed model (Table 2).
FIGURE 3 | De elopmen o chlo ophyll luo escence Ma ch
2013–Feb ua y 2014. Da ke blue and ed lines wi h ci cles indica e
measu emen s o needles ha bu s in sp ing 2012 o pine and sp uce,
espec i ely. B igh e lines wi h diamonds a e he co esponding alues o
needles ha bu s in sp ing 2013. E o ba s show he s anda d de ia ion o
measu emen s o each day.
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Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
The c osso e empe a u e pa ame e alue, which indica es
he empe a u e whe e he change o luo escen ac i i y is a i s
la ges , was lowe o sp uce compa ed o pine and also lowe
o sp ing needles (o “2012 needles”) compa ed o au umn nee-
dles (“2013 needles”) (Table 3,Figu e 4). This means ha o any
gi en empe a u e below he sa u a ing empe a u e, he pho o-
syn he ic ac i i y o sp uce is highe han ha o pine. Needles
we e mo e ac i e in au umn han du ing sp ing o bo h species.
The slope o luo escence de elopmen was s eepe o pine in he
sp ing. This sugges s a mo e apid de elopmen o pho osyn he ic
capaci y as empe a u es inc ease, which compensa es o some
o he e ec o he highe c osso e empe a u e. Acco ding o
he i ed models, di e ences in all o he pa ame e alues excep
o amin be ween species and needle o igins a e clea ly s a is ically
signi ican (p- alues <0.0001).
Models o indi idual ees show g ea e a ia ion o sp uce
han pine (Table 3,Figu e 4).Sp uce eeswe emo e a iable
in e ms o hei o igin, being d awn om h oughou Finland
(i.e., 60–66◦N) and loca ions in cen al Eu ope, while pines
all came om no he n Finland (Table 1). Howe e , associa ion
Table 2 | The log-likelihood alues o he mixed model wi h di e en
ime cons an alues o he mo ing mean and minimum daily
empe a u es.
Time cons an Log-likelihood
Days Mean empe a u e Minimum empe a u e
1 12.771 9428
2 14.029 11.476
3 14.359 12.546
4 14.545 13.483
5 14.648 14.094
6 14.692 14.339
7 14.695 14.432
8 14.669 14.457
9 14.621 14.439
10 14.559 14.393
11 14.486 14.326
12 14.407 14.243
Table 3 | Pa ame e es ima es and s anda d e o s (in pa en heses)
o he ixed e ec s in he non-linea mixed model using a 7-day
sliding a e age o daily mean empe a u e as a p edic o .
Pine (Pinus Sp uce (Picea abies
syl es is L) [L.] Ka s )
amax 0.847 (0.002) 0.833 (0.001)
amin 0.081 (0.003) 0.078 (0.006)
2012
(Sp ing)
c3.841 (0.081) −0.925 (0.318)
b2.181 (0.062) 3.834 (0.095)
2013
(Au umn)
c−1.647 (0.119) −10.765 (0.341)
b4.886 (0.106) 4.710 (0.122)
be ween he la i ude o o igin and c oss-o e empe a u e was no
s a is ically signi ican in ou da a (Figu e 5).
DISCUSSION
Ou measu emen s o chlo ophyll luo escence indica e ha he
ac i i y o pho osyn he ic ligh eac ions o bo eal coni e s ol-
lows ambien ai empe a u e. In sp ing 2013, F /Fm eached
FIGURE 4 | P edic ed chlo ophyll luo escence (F /Fm) as a unc ion o
empe a u e o he sp uce and pine needles (uppe and lowe ows,
espec i ely) and o he old and new needles (le and igh columns,
espec i ely). The hick lines show he a e age model o all ees in he
g oup, wi h hin lines indica ing indi idual ees. Figu es a e based on he
bes - i ing model using a 7-day sliding a e age o daily mean empe a u e.
FIGURE 5 | Associa ion be ween he la i ude o o igin and es ima ed
ee-speci ic c oss-o e empe a u e ci o sp uces in he sp ing (2012
needles). Spea man’s ank co ela ion ρ=−0.23 (p=0.10).
www. on ie sin.o g June 2014 | Volume 5 | A icle 264 |5

Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
minimum le els in Ma ch a e a cold pe iod o se e al weeks.
Ai empe a u es la e in 2013 and du ing Janua y–Feb ua y 2014
we e unusually wa m, up o 6◦C abo e he long- e m a e -
age (Figu e 1). Du ing his pe iod, F /Fm alues emained high,
wi h sp uce almos eaching le els obse ed du ing he sum-
me (Figu e 3). S udies o ne ecosys em exchange using eddy-
co a iance me hods (Van Dijk and Dolman, 2004; Vesala e al.,
2010) ha e shown ha ees main ain hei espi a ion du ing
such wa m bu da k pe iods, which sugges s ha pho osyn he ic
da k eac ions a e also ac i e du ing wa m spells in win e . The
low F /Fm alues obse ed a e he cold pe iod in Janua y 2014
indica e a down- egula ion o ligh eac ions. Ö lande (1993)
sugges ed ha his down- egula ion is due o damage o pho o-
sys em II caused by ligh ecep ion in sub eezing empe a u es.
Howe e , he No way sp uce and Sco s pine in ou common
ga den expe imen quickly eco e ed om his decline, and he
F /Fm a io ollowed he empe a u e inc ease. This indica es ha
pho osys em II o he coni e s can sus ain eeze- haw cycles o a
leas –20◦C, wi h apid eco e y du ing milde pe iods. No way
sp uce ended o main ain a highe F /Fm a io, and eac i a ed
as apidly as Sco s pine, which showed s onge pho oinhibi ion
du ing cold spells. Di e ences in he ac i i y o he pho osyn-
he ic appa a us can be linked o he way hese wo coni e s
down- egula e espi a ion. Ög en e al. (1997) showed ha cold
ole ance o coni e s is co ela ed wi h he soluble suga con en
o hei needles and ha No way sp uce is mo e os ole an
han Sco s pine o Lodgepole pine—a p oposal ha is in con lic
wi h esul s p esen ed he e. The au ho s also obse ed ha sp uce
down- egula ed espi a ion as e and mo e ex ensi ely han pine,
which imp o ed he conse a ion o suga s o age in sp uce.
Du ing he mild win e pe iod, ou sp uce ees exhibi ed con-
side ably highe alues o luo escence compa ed o pine. These
esul s e lec hose o Beuke e al. (1998), who es ed os ol-
e ance by exposing seedlings o a ange o eezing empe a u es
and measu ing he subsequen leakage o elec oly es. They ound
ha pine becomes os ole an much ea lie du ing he au umn,
loses i la e in he sp ing, and ole a es lowe empe a u es du -
ing he win e (Figu e 6, a ep oduc ion o Figu es 3, 6 in Beuke
e al., 1998). Se e al expe imen al s udies ha e shown ha os
esis ance and pho osyn he ic ac i i y a e linked (Leinonen, 1996;
Repo e al., 2000, 2006; Mäkelä e al., 2004). The e o e, he con-
clusions o Beuke e al. (1998) a e consis en wi h ou esul s.
We did no measu e ac ual needle empe a u es, as Ma in e al.
(1999) showed ha needle empe a u es o subalpine Paci ic sil-
e i a e ypically≤1◦C highe han ambien , and we assumed a
simila ela ionship was applicable in sou he n Finland.
In his s udy, he c osso e pa ame e alues (Table 3,
Figu e 3) we e lowe in he sp ing (i.e., 2012 needles) compa ed
o he au umn (i.e., 2013 needles) o bo h species. This indica es
a lowe ac i i y o ligh eac ions a any empe a u e in he sp ing
compa ed o he au umn. This ag ees wi h Repo e al. (2006),
who no ed ha he empe a u e-linked pho osyn he ic ac i i y is
FIGURE 6 | De elopmen o os esis ance o No way sp uce ( ed) and
Sco s pine (blue) buds h ough h ee win e s. The solid line shows he
daily mean empe a u e o he s udy pe iod. The igu e is a combina ion o
Figu es 3, 6 in Beuke e al. (1998) ( ep oduced wi h pe mission), who es ed
os esis ance by exposing seedlings o eezing empe a u es and
measu ing he subsequen leakage o elec oly es.
F on ie s in Plan Science | Func ional Plan Ecology June 2014 | Volume 5 | A icle 264 |6
Linkosalo e al. Di e ences in cold-inhibi ion o bo eal coni e s
di e en in au umn and sp ing and ha pho osyn he ic po en-
ial is highe in au umn compa ed o sp ing, when es ima ed wi h
ligh -sa u a ed assimila ion a e and he appa en quan um yield
achie ed wi h gas exchange measu emen s.
Resul s p esen ed he e indica e ha No way sp uce egains
he po en ial o pho osyn he ic ac i i y mo e apidly han Sco s
pine when empe a u es suddenly wa m du ing he cold mon hs.
The esul s disag ee wi h hose o Lundma k e al. (1988),who
sugges ed hese species o be simila in his espec . No way
sp uce is conside ed o be mo e p one o sp ing os damage
due o a p e e ence o os -p one si es and sensi i i y o new
shoo s (Lundma k and Hällg en, 1987). Ou esul s indica e ha
his sensi i i y is also a consequence o ea lie eac i a ion o
pho osyn hesis.
Because he Sco s pine in ou s udy had a mo e no he ly o i-
gin han heNo waysp uce,weexpec ed hepines obebe e
adap ed o cold and ha hey would s a pho osyn hesizing a
lowe empe a u es (Hänninen e al., 2007). Howe e , ou esul s
indica e ha pho osyn he ic eac i a ion was ac ually mo e con-
se a i e in pines. We conclude ha he di e ence be ween hese
wo coni e s is due o species-speci ic esponses o a common
en i onmen al change a he han a consequence o sample ee
p o enance. Mo eo e , sp uce ees we e d awn om a wide a ea
han he pines, so one would assume o igin explains some o he
a iance in he model pa ame e s o his species. Howe e , we
ound no s a is ically signi ican ela ionship be ween ee o igin
and pa ame e alues, and an explana ion o he g ea e a ia ion
obse ed o sp uce emains obscu e.
We es ed a ange o ime cons an alues om 1 o 12 days
when calcula ing he mo ing a e age o empe a u e. In he end,
he ime cons an had only a sligh e ec on model pe o mance.
The ime cons an , o esponse ime, is belie ed o e lec he a e
a which pho osyn he ic ac i i y eac s o changes in he en i-
onmen . Ea lie s udies ha e p oduced a wide ange o esponse
imes, e.g., 2 days (O ande and Öquis , 1991), 8 days (Kola i
e al., 2007), o up o 12 days (Mäkelä e al., 2004). Ou model i -
ed he da a sligh ly be e wi h a esponse ime o 7 days, bu wi h
only sligh di e ences in model pe o mance be ween one alue
and ano he , i is di icul o selec any speci ic alue. We suspec
ha he la dis ibu ion o model pe o mance o e a ange o
esponse imes accoun s o he wide ange o alues epo ed in
he li e a u e.
Di e ences in he phenology o pho osyn hesis be ween he
wo coni e species ha e impo an implica ions o modeling o -
es p oduc i i y and o es y planning in he u u e. Acco ding
o ou esul s, sp uce eac i a es he ligh eac ions o i s pho o-
syn hesis mo e easily. We specula e ha his implies ha sp uce
also mo e eadily eac i a es i s pho osyn hesis, and is he e o e
be e adap ed o u ilize he wa me sp ing empe a u es. On he
o he hand, ea lie onse o pho osyn he ic ac i i y also uns a
g ea e isk o os damage, especially i a ia ion in sp ing ime
daily empe a u es inc eases. Howe e , i daily empe a u e a i-
a ion emains simila o ha seen oday, No way sp uce will gain
an ad an age in a wa me u u e clima e. Ou model o pho osyn-
he ic ac i i y can be used in p ocess-based g ow h/yield models
o cha ac e ize he di e en pa e ns o pho osyn hesis and es-
pi a ion o sp uce and pine. I can also be used as a ool o
explo ing how he isk o os will de elop unde u u e clima e
scena ios and wea he pa e ns.
ACKNOWLEDGMENTS
This s udy was unded by he Academy o Finland as a pa
o he Finnish Resea ch P og am on Clima e 377 Change
(FICCA, p ojec numbe 140776). We would like o hank Raimo
Jaa inen a he Haapas ensy jä common ga den o managing
he luo escence measu emen s as well as Endika Be ojalbiz
Aldamize xeba ia, Bingen Chamo o Ama , Mo ane Cla el,
Thomas Desu mon , Ma ia Diez Alonso, Edua d Ibanez Salinas,
Al a o Jimenez Gonzalez, Theo Le Dan ec, Jussi Mäkelä, Ignacio
Ma in And es, Inigo Osua Fon u bel, and Clemence Waline o
conduc ing he ac ual measu emen s.
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Recei ed: 28 Ma ch 2014; accep ed: 21 May 2014; published online: 13 June 2014.
Ci a ion: Linkosalo T, Heikkinen J, Pulkkinen P and Mäkipää R (2014) Fluo escence
measu emen s show s onge cold inhibi ion o pho osyn he ic ligh eac ions in Sco s
pine compa ed o No way sp uce as well as du ing sp ing compa ed o au umn. F on .
Plan Sci. 5:264. doi: 10.3389/ pls.2014.00264
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