F on ie s in Fo es s and Global Change 01 on ie sin.o g
Reduced g ow h sensi i i y o
wa e a ailabili y as po en ial
indica o o d ough -induced ee
mo ali y isk in a Medi e anean
Pinus syl es is L. o es
Asie He e o
1
*, RaquelGonzález-Gascueña
2,
Pa iciaGonzález-Díaz
3, PalomaRuiz-Beni o
4 and
En iqueAndi ia
2
1 FisioKlima-Ag oSosT Resea ch G oup, Plan Biology and Ecology Depa men , Facul y o Pha macy,
Uni e si y o he Basque Coun y, UPV-EHU, Vi o ia-Gas eiz, Spain, 2 Depa men o Biodi e si y,
Ecology and E olu ion, Facul y o Biological Sciences, Uni e sidad Complu ense de Mad id, Mad id,
Spain, 3 Cen o de In es igaciones sob e Dese i icación (CIDE, CSIC-UV-GV), Valencia, Spain, 4 G upo
de Ecología y Res au ación Fo es al (FORECO), Depa amen o de Ciencias de la Vida, Uni e sidad de
Alcalá, Mad id, Spain
In oduc ion: D ough -associa ed ee mo ali y has been inc easing wo ldwide
since he las decades, impac ing s uc u e and unc ioning o o es ecosys ems,
wi h implica ions o ene gy, ca bon and wa e luxes. Howe e , he unde s anding
o he indi idual ulne abili y o d ough -induced mo ali y is s ill limi ed.
Me hods: We aimed o iden i y he ac o s ha igge ed he mo ali y o he
widely dis ibu ed Pinus syl es is L. in an ex ensi e o es a ea in cen al Spain.
We compa ed adial g ow h pa e ns in pai s o ali e and ecen ly dead indi iduals
ha co-occu in close p oximi y and p esen simila age and size, he eby
isola ing he e ec s o size and en i onmen om he mo ali y p ocess. Tempo al
dynamics o g ow h, g ow h synch ony, and g ow h sensi i i y o wa e a ailabili y
(p ecipi a ion minus po en ial e apo anspi a ion) we e compa ed be ween ali e
and ecen ly dead ees.
Resul s and discussion: O e he las 50 yea s, al hough we did no de ec
signi ican di e ences in g ow h be ween ali e and dead ees, an inc ease in he
g ow h synch ony and sensi i i y o wa e a ailabili y (i.e. slope o he clima ic
wa e balance in he g ow h model) was obse ed in all ees as d ough in ensi y
inc eased. 20 yea s be o e mo ali y, dead indi iduals showed lowe g ow h
synch ony and g ow h sensi i i y o wa e a ailabili y han ali e ones, wi hou
signi ican di e ences in g ow h. Reco ded educ ion in g ow h synch ony and
g ow h sensi i i y o wa e a ailabili y in dead ees sugges s a decoupling be ween
ee g ow h and clima e, which could inc ease he isk o hyd aulic ailu e and/
o ca bon s a a ion unde inc easingly a id condi ions. Thus, he use o educed
g ow h sensi i i y o wa e a ailabili y as po en ial ea ly-wa ning signal o ee
mo ali y, oge he wi h educed g ow h synch ony, should be u he explo ed,
pa icula ly in pine species in seasonally d y a eas.
KEYWORDS
clima e change, dend oecology, synch ony, ulne abili y, sco s pine, ee die-o ,
clima ic wa e balance
OPEN ACCESS
EDITED BY
E win D eye ,
INRA Cen e Nancy-Lo aine, F ance
REVIEWED BY
Ma hieu Lé esque,
ETH Zü ich, Swi ze land
Maxime Caille e ,
Ins i u Na ional de eche che pou
l’ag icul u e, l’alimen a ion e l’en i onnemen
(INRAE), F ance
*CORRESPONDENCE
Asie He e o
asie [email p o ec ed]
RECEIVED 28 June 2023
ACCEPTED 24 Oc obe 2023
PUBLISHED 09 No embe 2023
CITATION
He e o A, González-Gascueña R,
González-Díaz P, Ruiz-Beni o P and
Andi ia E (2023) Reduced g ow h sensi i i y o
wa e a ailabili y as po en ial indica o o
d ough -induced ee mo ali y isk in a
Medi e anean Pinus syl es is L. o es .
F on . Fo . Glob. Change 6:1249246.
doi: 10.3389/ gc.2023.1249246
COPYRIGHT
© 2023 He e o, González-Gascueña,
González-Díaz, Ruiz-Beni o and Andi ia. This is
an open-access a icle dis ibu ed unde he
e ms o he C ea i e Commons A ibu ion
License (CC BY). The use, dis ibu ion o
ep oduc ion in o he o ums is pe mi ed,
p o ided he o iginal au ho (s) and he
copy igh owne (s) a e c edi ed and ha he
o iginal publica ion in his jou nal is ci ed, in
acco dance wi h accep ed academic p ac ice.
No use, dis ibu ion o ep oduc ion is
pe mi ed which does no comply wi h hese
e ms.
TYPE O iginal Resea ch
PUBLISHED 09 No embe 2023
DOI 10.3389/ gc.2023.1249246
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 02 on ie sin.o g
1. In oduc ion
The widesp ead inc ease in ee mo ali y has become one o he
mos se ious h ea s o o es ecosys ems wo ldwide o e he pas ew
decades (Allen e al., 2010; Milla and S ephenson, 2015; G eenwood
e al., 2017). Inc eased a idi y, along wi h ex eme d ough s and hea
wa es ha e been iden i ied as he main d i e s o ee mo ali y (Pa k
Williams e al., 2013; Ruiz-Beni o e al., 2013; Hammond e al., 2022).
Mo eo e , bo h human managemen legacies and bio ic agen s can
in e ac wi h clima ic s esso s, u he inc easing ee mo ali y
(Lina es e al., 2010; Ande egg e al., 2015; Sangüesa-Ba eda e al.,
2015; McDowell e al., 2022). The impac o inc easing ee mo ali y,
pa icula ly in he o m o massi e mo ali y e en s, ex ends beyond
indi idual ees and can ha e a - eaching e ec s on ecological
communi ies, ecosys em unc ioning and se ices, and land-clima e
in e ac ions (Ande egg e al., 2013). High ee mo ali y can al e
species composi ion and dis ibu ion, and ul ima ely shi s o es
communi ies owa ds highe dominance o sh ub species (Allen and
B eshea s, 1998; Peñuelas e al., 2007; He e o e al., 2013; He e o and
Zamo a, 2014; Allen e al., 2015; Ruiz-Beni o e al., 2017). The loss o
ee co e can also ha e signi ican implica ions o ene gy, ca bon and
wa e luxes, and nu ien cycling (Hughes e al., 2006; Allen, 2007;
Roye e al., 2011; Xiong e al., 2011; Ande egg e al., 2013).
The cu en impo ance o ee mo ali y in o es unc ioning and
esilience igge ed he s udy o he ee mo ali y p ocess (e.g.,
McDowell e al., 2022). Howe e , he unde s anding o unde lying
mechanisms o ee mo ali y and he de elopmen o obus ea ly-
wa ning indica o s emain limi ed due o complex in e ac ions
be ween d i e s and in ol ed p ocesses (Cama e o e al., 2015;
Caille e e al., 2017; Ha mann e al., 2018; McDowell e al., 2022).
T ee mo ali y has been widely linked o hyd aulic ailu e and ca bon
s a a ion, wi h e idence sugges ing ha hey a e no mu ually
exclusi e bu in e dependen (McDowell e al., 2011). In his ega d,
dend oecology p o ides aluable in o ma ion o un a el he
physiological mechanisms behind ee mo ali y and o de elop ea ly
wa ning indica o s (Caille e e al., 2017; Ha mann e al., 2018).
Dend oecological s udies allow o easy obse a ion o g ow h a es,
widely used as an indica o o ee i ali y (Dobbe in, 2005), o
almos he en i e li espan o sampled indi iduals ac oss ex ensi e
a eas, which is key o assessing clima ic e ec s on ee unc ioning.
Addi ionally, synch ony in adial g ow h, de ined as coinciden
inc eases o dec eases in adial g ow h o e ime ac oss indi iduals in
a single popula ion, has been widely used as a sign o o es
ulne abili y o clima e change. In his con ex , high coincidence in
g ow h pa e ns be ween indi iduals (i.e., highe co ela ion in ee
g ow h among indi iduals) e eals he s ong impac o clima ic
s esso s (Boden e al., 2014; Shes ako a e al., 2016). O e all, he
s udy o empo al changes in ee g ow h esponses o d ough and
wa ming can p o ide insigh s in o indi idual ee p edisposi ion
o mo ali y.
The compa ison o g ow h pa e ns be ween co-occu ing dead
and su i ing ees has become a common me hod o unde s anding
and modelling ee mo ali y (Pede sen, 1998; Ogle e al., 2000;
Caille e e al., 2017). In many cases, a decline in g ow h p io o
mo ali y has been obse ed, al hough he magni ude and du a ion o
his decline a ied depending on species’ unc ional cha ac e is ics
and ac o s d i ing mo ali y (Gea-Izquie do e al., 2014, 2019;
Caille e e al., 2017). Fo example, while d ough - ole an species and
ees ha died due o compe i ion showed s ong and long-las ing
g ow h declines, ees ha died om bio ic a acks o en showed small
and sho - e m educ ions (Caille e e al., 2017). G ow h pa e ns
p io o mo ali y can p o ide aluable in o ma ion on he
physiological mechanisms unde lying he mo ali y p ocess, as
changes in ee unc ion (e.g., hyd aulic conduc i i y) and s uc u e
(e.g., lea a ea) a ec ing ee g ow h o en p ecede mo ali y
(McDowell e al., 2011; Seidl e al., 2011). G ow h synch ony can also
se e as an ea ly wa ning indica o o mo ali y. Fo example, Caille e
e al. (2019) showed a dec ease in he synch ony o gymnospe m
species 20 yea s be o e mo ali y. Howe e , o make compa isons
be ween ali e and dead ees mo e obus , i is essen ial o s anda dize
a iables ha may a ec adial g ow h and i s a iabili y, such as ee
size and bio ic and abio ic e ec s (Muñoz-Gál ez e al., 2021; Neycken
e al., 2022). S udies ha compa e g ow h pa e ns be ween ali e and
dead ees while con olling o hese key a iables may p o ide new
insigh s in o possible g ow h-based ea ly wa ning indica o s. Gi en
he wide a ie y o species and popula ion esponses, ypes o clima ic
s ess, and combina ions o mo ali y d i e s (Caille e e al., 2017), i
is necessa y o ake ad an age o as many ee die-o e en s as possible
in o de o e ine and expand he exis ing knowledge ega ding he
ee mo ali y p ocess and mo ali y isk indica o s.
T ee species a he limi s o hei dis ibu ion, such as empe a e
o bo eal species in d ough -p one Medi e anean a eas, o en ace
pa icula ly ad e se ecological condi ions (Hampe and Pe i , 2005;
Hampe and Jump, 2011). This could beagg a a ed by he inc easing
magni ude and equency o ex eme d ough e en s in Medi e anean
a eas p ojec ed by clima e change scena ios (IPCC, 2021), making
empe a e and bo eal species g owing in Medi e anean a eas
especially ulne able o d ough -induced mo ali y (Galiano e al.,
2010; He e o e al., 2013; Vila-Cab e a e al., 2013). Fu he mo e,
e o es a ion and a o es a ion, and he abandonmen o adi ional
o es managemen p ac ices (e.g., ee ha es o wood uel and
o es clea ing o ca le anching) ha e inc eased he densi y o many
Medi e anean o es s, leading o inc eased in e -indi idual
compe i ion o wa e esou ces (Lina es e al., 2010; Vila-Cab e a
e al., 2013) and ul ima ely o o es decline and mo ali y e en s
(Ma ínez-Vilal a and Pinol, 2002; Galiano e al., 2010; Vila-Cab e a
e al., 2013; Gazol and Cama e o, 2022). In his con ex , he e is a
c i ical need o s udy g ow h-based ea ly-wa ning indica o s o
mo ali y in ee species’ ea -edge popula ions in Medi e anean
a eas, which can aid in implemen ing o es managemen and
biodi e si y conse a ion ac ions o he adap a ion o hese
ecosys ems o clima e change.
In his s udy, we in es iga ed g ow h-based mo ali y isk
indica o s in Sco s pine (Pinus syl es is L.) ees in a high-densi y
o es in Cen al Spain. P. syl es is is an economically impo an and
widely dis ibu ed bo eo-alpine species in Eu ope (Ba bé o e al.,
1998), wi h i s sou he nmos limi in he Ibe ian Peninsula whe e i
has expe ienced ecen mo ali y e en s (Galiano e al., 2010; Vila-
Cab e a e al., 2013). Fo his, we(i) e alua ed he e ec s o in insic
( ee size), bio ic (compe i ion) and abio ic (wa e a ailabili y)
ac o s, and s a us (dead/ali e) on he g ow h a es, (ii) analyzed he
empo al pa e n o g ow h sensi i i y o wa e a ailabili y compa ing
dead and ali e ees, and (iii) quan i ied g ow h synch ony compa ing
dead and ali e ees. By doing so, wesough o gain insigh s in o he
mechanisms unde lying ee mo ali y and help o de elop a eliable
g ow h-based mo ali y isk indica o o P. syl es is in
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 03 on ie sin.o g
Medi e anean a eas. In ag eemen wi h p e ious indings in
gymnospe m species, weexpec lowe g ow h a es in dead han in
su i ing ees be o e mo ali y, likely due o hei isohyd ic wa e
egula ion (Salmon e al., 2015; Caille e e al., 2017). Fu he mo e,
wean icipa e ha compe i ion had a g ea e impac on g ow h in
dead ees, which could in ensi y he ad e se impac o d ough
(Lina es e al., 2010). Finally, wealso expec a dec ease in g ow h
synch ony in dead ees be o e mo ali y (Caille e e al., 2019),
sugges ing a misma ch be ween g ow h and high- equency
clima ic luc ua ions.
2. Ma e ials and me hods
2.1. S udy a ea
The s udy a ea is an ex ensi e pine o es loca ed in he Al o Tajo
Na u al Pa k o cen al Spain a an ele a ion o 1,450–1,600 m a.s.l.
(40° 39′ 6.8″N, 1° 41′ 53.1″W). This o es expe ienced a widesp ead
ee mo ali y e en du ing 2016 and 2017. No sign o bio ic agen s
was de ec ed. The o es a ea is domina ed by P. syl es is. The soil ype
in he a ea is p ima ily calcium cambisols (Ma ín-Mo eno e al.,
2014). The s udy a ea is submi ed o a con inen al Medi e anean
clima e wi h cold win e s and mild and d y summe s, wi h a mean
annual empe a u e o 10.5°C and a mean annual o al p ecipi a ion
o 468 mm (pe iod 1948–2017), acco ding o da a om a
me eo ological s a ion o AEMET (Spanish Me eo ological Agency)
loca ed a Molina de A agón, which is si ua ed 25 km om he
s udy a ea.
2.2. Sampling design and
dend och onological me hods
Du ing Oc obe 2017, wesampled 39 pai s o ees wi hin he
s udy a ea. Fo each pai , one ee was obse ed o bein a heal hy s a e
(wi h no signs o decline), while he o he was dead, bu wi h d y
needles s ill p esen in he c own indica ing ecen mo ali y. T ee
mo ali y was con i med in he ollowing yea s. The sampled pai s had
simila size and hey we e loca ed no mo e han 5 me e s apa om
each o he (wi h an a e age dis ance o 3 me e s). Two co es we e
aken om each ee in opposi e di ec ions using a P essle inc emen
bo e . The diame e a b eas heigh (DBH) o each sampled ee was
also eco ded, along wi h he DBH o e e y neighbo ing adul ee
(i.e., DBH > 7.5 cm, heigh > 130 cm) wi hin a ci cula plo o 10 me e s
adius measu ed om he a ge ees.
Co es we e p ocessed ollowing s anda d ecological me hods
(F i s, 1976). They we e ai -d ied o 48–72 h, moun ed on wooden
suppo s, and sanded wi h p og essi ely ine g ades o sandpape o
highligh ing-wid h pa e ns. All co es we e isually c oss-da ed
ollowing he p ocedu es desc ibed by Yamaguchi (1991). Co es we e
scanned a 1,200 dpi esolu ion (EPSON Pe ec ion 800) and ee-
ing wid h was measu ed using Image J so wa e (Schneide e al.,
2012). T ees can die du ing he g owing season be o e ing o ma ion
is comple e, which induces an incomple e ou e mos ing. As ee
could ha e died a di e en imes du ing he 2017 g owing season,
wedid no conside he las ing o sampled ees (Caille e e al.,
2017). Ring wid h was con e ed o basal a ea inc emen (BAI, cm
2
yea
−1
) assuming a ci cula s em c oss-sec ion and using he
ollowing o mula:
22
1
()
BAI
π
−
= −
whe e
and
-1
a e he adius o he ee a he end and a he
beginning o a gi en annual ing, espec i ely. Fo each ee and yea ,
he BAI was calcula ed as an a e age o he wo ex ac ed co es. BAI
is a meaning ul indica o o ee g ow h as i emo es he a ia ion in
g ow h due o inc easing ci cum e ence, making i mo e ela ed o
biomass inc emen han ing wid h (Biondi and Qeadan, 2008).
To quan i y in e -indi idual compe i ion in sampled ees,
wecalcula ed he Lo ime ’s compe i ion index (CI, Lo ime , 1983)
using he ollowing o mula:
CI BA
BA
i
=∑
whe e BA
i
is he basal a ea o each neighbo ee wi hin he
ci cula plo o 10 m adius and BA is he basal a ea o he a ge ee.
Weemployed he dis ance-independen Lo ime ’s compe i ion index,
since i is app op ia e o measu e compe i ion in monospeci ic o es s
(Kan a Bhanda i e al., 2023 and e e ences wi hin) and has been
p e iously used in Medi e anean a eas (e.g., Muñoz-Gál ez
e al., 2021).
2.3. Wa e a ailabili y
To quan i y he annual wa e a ailabili y, wecalcula ed he annual
clima ic wa e balance by sub ac ing he annual po en ial
e apo anspi a ion (PET) om he o al annual p ecipi a ion (P). The
PET was de e mined ollowing he me hod p oposed by Tho n hwai e
(1948). To accoun o he in luence o p e ious yea condi ions on he
cu en g owing season, wecalcula ed annual clima ic wa e balance
om Oc obe o he p e ious yea o Sep embe o he p esen yea .
P e ious au umn and win e p ecipi a ion can play an impo an ole
echa ging soil wa e ese es, and can boos cu en yea adial
g ow h in P. syl es is (Sánchez-Salgue o e al., 2012). Weused clima ic
da a om he AEMET me eo ological s a ion a Molina de A agón.
2.4. Da a analysis
We used a linea mixed-e ec model o compa e BAI se ies
be ween ali e and dead ees and assess he e ec o ee size,
compe i ion and wa e a ailabili y on ee g ow h du ing he 1948–
2017 pe iod (a pe iod selec ed o inc ease sample size). Weincluded
ee iden i y nes ed wi hin ee-pai s as a andom e ec o accoun o
he epea ed measu emen s on he ali e/dead pai ed indi iduals.
Wealso used an au o eg essi e s uc u e o conside he empo al
au oco ela ion o successi e annual g ow h inc emen s (Pinhei o
e al., 2018). T ee size (DBH a he beginning o each yea ),
compe i ion (CI), wa e a ailabili y (P-PET), s a us (ali e s. dead),
and he in e ac ions s a us × compe i ion and s a us × wa e
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 04 on ie sin.o g
a ailabili y we e conside ed as ixed e ec s in he model. Size was
included as a second-deg ee polynomial o allow o nonlinea
esponses o g ow h o a ia ions in size (Sumida e al., 2013). All he
a iables we e s anda dized by sub ac ing om i s sample mean and
by di iding by i s s anda d de ia ion.
In o de o assess he empo al a ia ion o g ow h sensi i i y o
wa e a ailabili y in bo h ali e and dead ees weused he mixed e ec
model desc ibed abo e. The model was i ed o 5-yea lagged
windows o 20 yea s (Díaz-Ma ínez e al., 2023; i.e., 11 ime-windows
o 20 yea s wi h a s a ing yea om 1948 o 1998).
To assess g ow h synch ony wi hin ali e and dead ees
we ollowed he p ocedu e desc ibed by Alday e al. (2018). B ie ly,
weused a iance–co a iance mixed modelling using yea as andom
e m and calcula ed he mean in e -ch onology co ela ion (i.e.,
g ow h synch ony) as he common in e -annual g ow h a iance o
all dead and ali e ees. To do his, we es ed di e en a iance–
co a iance s uc u es (see Alday e al., 2018 o a comple e o e iew
o a iance–co a iance s uc u es) ha allow o cha ac e ize
synch ony o each le el o he g ouping a iable (i.e., dead and ali e
ees). The bes a iance–co a iance s uc u e was selec ed using he
Akaike In o ma ion C i e ion (AIC, Zuu e al., 2009). The empo al
changes in g ow h synch ony o ali e and dead ees we e also
assessed using 20-yea in e als wi h a 5-yea mo ing window.
All s a is ical analyses we e done in R 4.1.3 (R Co e Team, 2022)
using he nlme (Pinhei o e al., 2018), MuMIn (Ba on, 2019) and R
Dend oSync (Alday e al., 2018) packages.
3. Resul s
3.1. Cha ac e is ics o sampled ees
Conside ing aw g ow h da a (BAI) o he 1900–2017 pe iod,
ali e and dead ees showed simila pa e ns along he 1900–2017
pe iod, ye ali e ees showed signi ican ly lowe mean BAI han dead
ees (Table1), especially be ween 1930 and 1980 (Figu e1). A e
1980s, ali e and dead ees showed simila g ow h a es, excep in he
las yea s when dead ees also showed g ea e g ow h han ali e ees
(Figu e1). No signi ican di e ences we e ound o age, size (DBH),
compe i ion index (CI) and su ounding basal a ea o sampled
indi iduals (BA) be ween ali e and dead ees (Table1). All sampled
ees p esen ed an a e age age o 130 yea s and a e age DBH o 34 cm
(Table1).
3.2. E ec o size, compe i ion and clima e
on g ow h
T ee adial g ow h was signi ican ly in luenced by ee size
(F = 86.74, p < 0.001), compe i ion index (F = 7.35, p = 0.01), wa e
a ailabili y (F = 207.11, p < 0.001) and i s in e ac ion wi h ee s a us
(i.e., ali e o dead; F = 8.97, p < 0.01). O e all, no signi ican di e ences
we e ound on ee g ow h be ween ali e and dead ees o he 1948–
2017 pe iod (F = 1.98, p = 0.17; Table 2). Howe e , when wa e
a ailabili y was low, dead ees showed g ea e g ow h han li e ees
(Figu e2). Compe i ion had a nega i e e ec on g ow h, whe eas he
e ec o he wa e a ailabili y was posi i e (Table 2). Dead ees
showed signi ican ly less sensi i i y o wa e a ailabili y (lowe slope)
han ali e ees.
3.3. Tempo al changes in g ow h pa e ns
Time windows analysis showed simila g ow h pa e ns be ween
li e and dead ees o he s udied pe iod (Figu e 3;
Supplemen a y Table S1).
G ow h sensi i i y o wa e a ailabili y inc eased along he s udy
pe iod, coinciding wi h a dec ease in wa e a ailabili y (Figu e4).
Ali e ees showed g ea e sensi i i y han dead ees du ing he i s
hal o he s udy pe iod. Howe e , his di e ence disappea ed, as wa e
a ailabili y dec eased, un il he las wo 20-yea in e als, when dead
ees showed lowe g ow h sensi i i y o wa e a ailabili y han ali e
ones (Figu e4).
3.4. G ow h synch ony
The bes - i a iance–co a iance s uc u e o calcula ing
synch ony was a he e ocedas ic ma ix wi h a composi e symme y
s uc u e (mHeCS; Supplemen a y Table S2). Fi s ly, he selec ion o
a he e ocedas ic ma ix implies ha he magni ude o he common
g ow h signal (i.e., g ow h synch ony) a ied signi ican ly be ween
li e and dead ees. Secondly, a ma ix wi h a symme ical s uc u e
sugges s he exis ence o luc ua ions in g ow h ha we e common o
bo h li e and dead ees. O e all, ali e ees exhibi ed signi ican ly
highe synch ony han dead ones (0.23 ± 0.03 and 0.16 ± 0.02,
espec i ely).
Rega ding empo al changes in synch ony, g ow h synch ony
alues we e ela i ely low un il he las 30 yea s, when a s eep inc ease
in synch ony was eco ded (Figu e5). The synch ony alues o ali e
and dead ees di e ged ma kedly du ing wo pe iods: in he second
qua e o he s udy pe iod and in he las in e al analyzed (jus
be o e he mo ali y e en ; Figu e5).
4. Discussion
Ou s udy e ealed signi ican di e ences be ween ali e and dead
ees in g ow h- ela ed pa ame e s unde a con ex o inc easing
a idi y. Bo h, g ow h sensi i i y o wa e a ailabili y and synch ony
we e lowe in dead han in ali e ees be o e mo ali y. This sugges s
a decoupling o ee g ow h om clima ic luc ua ions in dead ees
ha may ha e inc eased hei isk o sudden dea h due o hyd aulic
TABLE1 Cha ac e is ics o he sampled ees (mean ± SD).
All Li e Dead
BAI (cm2)5.33 ± 4.42 4.81 ± 3.89a5.84 ± 4.84b
Age a b eas
heigh (yea s)
129.96 ± 40.53 127 ± 44a133 ± 37b
DBH (cm) 33.97 ± 7.17 33.51 ± 7.3 34.30 ± 7.14
BA (m2ha−1)26.93 ± 10.88 26.83 ± 11.64 27.27 ± 8.03
CI 13.79 ± 10.33 14.15 ± 11.24 12.50 ± 6.34
BAI, Basal A ea Inc emen (1900–2017); DBH, Diame e a B eas Heigh (1.3 m); BA, Basal
A ea o he 10 m adius neighbo hood a ound he a ge ee; and CI, Lo ime ’s Compe i ion
Index. Le e s indica e signi ican di e ences be ween g oups (p< 0.05, pai ed - es ).
asigni ican di e ences be ween g oups (ali e and dead) o BAI. bsigni ican di e ences
be ween g oups (ali e and dead) o BAI.
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 05 on ie sin.o g
ailu e and/o ca bon s a a ion. Thus, educ ions in g ow h sensi i i y
o wa e a ailabili y, oge he wi h dec eased ee g ow h synch ony,
should also be conside ed as an ea ly-wa ning indica o o ee
mo ali y in Medi e anean P. syl es is popula ions loca ed a he
sou he n dis ibu ion limi o he species.
Con a y o ou i s hypo hesis, ou s udy did no ind lowe
g ow h in dead han in ali e ees p io o mo ali y, no a sus ained
dec ease in g ow h in dead ees o any o he appa en signs o g ow h
decline. These esul s con as wi h hose epo ed by Caille e e al.
(2017) o se e al gymnospe m species. Ne e heless, ou esul s a e
consis en wi h o he s udies ha ha e ound no di e ences be ween
dead and ali e ees a s and and egional scales (Fe enbe g e al.,
2014; Rowland e al., 2015; Be danie and Cla k, 2016; He guido e al.,
2016). When conside ing ou design based on dead/ali e ee pai s,
he e was no signi ican di e ence in g ow h be ween dead and ali e
ees du ing he i s 50 yea s o li e (da a no shown), uling ou he
possibili y ha mo ali y was due o a ade-o be ween ea ly-g ow h
and longe i y (Bigle e al., 2007; Bigle and Veblen, 2009).
Addi ionally, he size o ali e and dead ees s udied was simila .
The e o e, we a gue ha dead ees could ha e p io i ized adial
g ow h (o e o he ee unc ions) un il dea h ega dless o
en i onmen al s ess, o ha mo ali y occu ed ab up ly due o an
ex eme en i onmen al s ess leading o ee dea h wi hou a p e ious
impac on i s ca bon balance (Caille e e al., 2017).
We ound ha he e ec o wa e a ailabili y on g ow h a ied
be ween ali e and dead ees, wi h he la e showing highe g ow h
du ing ex emely d y condi ions (i.e., lowe g ow h sensi i i y o
wa e a ailabili y). Thus, unde se e e d ough condi ions, dead ees
may exhibi a less conse a i e wa e use han li e ees, which could
expose hem o a highe isk o hyd aulic ailu e due o he
accumula ion o enbolisms in he xylem (McDowell e al., 2022). Ou
esul s con as wi h p e ious s udies on P. syl es is, which showed
g ea e sensi i i y o d ough and ho condi ions o dead ees and a
sus ained decline in g ow h (He eş e al., 2012). Howe e , ou esul s
a e consis en wi h p e ious s udies pe o med on saplings, whe e
P. syl e s is appea s unable o dec ease i s heigh g ow h h ough
mo e s ic s oma al con ol unde ex eme d ough condi ions
(He e o e al., 2013). These di e ences in g ow h esponses o
d ough condi ions in dead ees be ween s udies may bedue o
in aspeci ic a iabili y and he in ensi y and ecu ence o d ough
e en s (Caille e e al., 2017).
We did no ind suppo o a g ea e impac o compe i ion on
g ow h in dead han ali e ees. Ou esul s showed ha nega i e
e ec s o compe i ion on ee g ow h we e simila o ali e and dead
FIGURE1
Basal A ea Inc emen (BAI, cm2, ± SE) o ali e and dead ees e alua ed o he 1900–2017 pe iod.
TABLE2 G ow h model pa ame e s (mean ± s anda d e o s).
Value S anda d e o d - alue p- alue
In e cep (s a e = dead) 1.749 0.049 5,152 35.320 0.0000
Poly (size) 1 19.687 1.886 5,152 10.434 0.0000
Poly (size) 2 −11.158 1.524 5,152 −7.319 0.0000
S a e (li e) −0.066 0.053 35 −1.245 0.2213
P-PET 0.037 0.005 5,152 8.005 0.0000
LCI −0.126 0.049 35 −2.533 0.0160
S a e (li e)*P-PET 0.020 0.007 5,152 2.995 0.0028
S a e (li e)*CI 0.026 0.054 35 0.494 0.6244
I includes he e ec o he size as a second-deg ee polynomial ans o ma ion [size poly (1) and size poly (2)], he wa e a ailabili y (P-PET), he compe i ion index (CI) and he in e ac ion
be ween s a us (ali e o dead) and wa e a ailabili y. The in e cep e e s o dead ees. Deg ees o eedom (d ), - alue and p obabili ies a e gi en.
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 06 on ie sin.o g
ees, as well as he in e -indi idual compe i ion index (CI), which
sugges s a limi ed e ec o compe i ion on he mo ali y e en .
None heless, he consis en nega i e e ec o compe i ion on adial
g ow h o ali e and dead ees sugges s he key ole o compe i ion on
exace ba ing d ough impac s on Medi e anean o es s (Lina es e al.,
2010; Vila-Cab e a e al., 2013). Howe e , i should beno ed ha
weused a s a ic compe i ion index measu ed a sampling, so i can no
e lec he e ec o compe i ion on he en i e g ow h se ies. This
ep esen s an impo an limi a ion in cla i ying he ole ha
compe i ion may play in d ough -induced g ow h educ ions o e
ime (Ma qués e al., 2021).
The s udy a ea expe ienced a p og essi e dec ease in wa e
a ailabili y o e ime. As d ough condi ions in ensi ied, sampled
ees inc eased hei g ow h sensi i i y o wa e a ailabili y. Howe e ,
a he beginning and a he end o he s udy pe iod, dead ees
showed lowe sensi i i y o wa e a ailabili y, indica ing po en ial
di e ences in physiological esponses o wa e s ess be ween ali e
and dead indi iduals. Lowe g ow h sensi i i y o wa e a ailabili y
p eceding mo ali y implies lowe s oma al esponsi eness, which
can lead o highe s oma al conduc ance and wa e use unde d y
condi ions as con i med by highe g ow h o dead ees unde low
wa e a ailabili y condi ions. This exposes ees o highe isk o
xylem embolism, inc easing he p obabili y o d ough -induced
hyd aulic ailu e h ough accumula ion o ca i a ion p ocesses
(McDowell e al., 2008, 2022). The g adual inc ease in a idi y may
ha e pushed indi iduals close o h eshold alues whe e ca i a ion
p ocesses occu . Howe e , he in e dependence o wa e and ca bon
luxes in ee unc ioning and igo p eclude us o exclude ca bon
s a a ion as he main mechanism in ol ed in he mo ali y p ocess
(McDowell e al., 2022). Rising empe a u es inc ease espi a ion
cos s, dec easing e en mo e he ca bon supply o ee unc ions
du ing d y pe iods o low ca bon assimila ion (Adams e al., 2009;
McDowell e al., 2011). Also, he less conse a i e wa e use
associa ed o lowe g ow h sensi i i y o wa e a ailabili y could
inc ease ee alloca ion o abo eg ound biomass (pa icula ly lea
a ea) du ing a o able condi ions, which canno behyd aulically and
me abolically sus ained du ing ex eme and ho d ough s (i.e.,
s uc u al o e shoo , Jump e al., 2017). The e o e, in his con ex o
FIGURE2
P edic ed g ow h esponse (BAI, cm2, ± SE) o wa e a ailabili y
(P-PET) o he pe iod 1948–2017in dead and ali e ees.
FIGURE3
P edic ed empo al g ow h e olu ion (BAI, cm2, ± SE) in ali e and
dead ees o he 1948–2017 pe iod applying he model a 20-yea
in e als wi h a 5-yea mo ing window. The yea s appea ing on he
x-axis co espond o he midpoin s o each 20-yea in e al.
FIGURE4
Tempo al e olu ion o (A) p edic ed (± SE) g ow h sensi i i y o wa e
a ailabili y (i.e., slope o clima ic wa e balance in he g ow h model)
in dead and ali e ees, and o (B) he wa e a ailabili y (P-PET) o he
1948–2017 pe iod. Da a a e showed o 20-yea in e als wi h a
5-yea s mo ing window. The yea s appea ing on he x-axis
co espond o he midpoin s o each 20-yea in e al.
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 07 on ie sin.o g
inc easing a idi y, educed sensi i i y o g ow h o wa e a ailabili y
may inc ease he isk o d ough mo ali y and could beused as an
ea ly-wa ning signal o ee mo ali y.
The obse ed pa e ns o inc eased g ow h synch ony o e ime
a e simila o he inc eased sensi i i y o wa e a ailabili y. In ac ,
highe g ow h sensi i i y could explain, in pa , he inc ease in g ow h
synch ony, since ee g ow h would bemo e and mo e linked o wa e
a ailabili y as condi ions becomes p og essi ely d ie , homogenizing
g ow h esponses ac oss he popula ion. The obse ed inc ease in
g ow h synch ony is consis en wi h p e ious s udies a local and
egional scales eco ding pe asi e clima ic e ec s on ee g ow h
(Boden e al., 2014; Shes ako a e al., 2016; Gazol e al., 2020). Ac ually,
inc eased synch ony is conside ed an indica o o ee ulne abili y o
clima e change, as i educes indi idual a iabili y and esilience
capaci y a popula ion le el (Cla k e al., 2012; Tejedo e al., 2020).
Tha is, inc eased g ow h synch ony o clima ic s esso s ampli y he
isk o ex ensi e nega i e impac s on ee igo a popula ion le el. In
his con ex o inc eased a idi y and ulne abili y a indi idual and
popula ion le els, di e ences in g ow h esponses be ween indi iduals
could play a key ole in mo ali y isk h ough he a o emen ioned
suscep ibili y o xylem embolism and dec eased ca bon supply o ee
unc ions. The e o e, unde d ie condi ions ees would beclose o
h eshold alues ela ed o key ee unc ions (e.g., s oma al
conduc ance) leading o pe manen d ough -induced damage, and
ul ima ely o ee dea h. F om his pe spec i e, and in line wi h ou
hi d hypo hesis, lowe synch ony was obse ed in dead ees bo h
p io o he mo ali y e en and du ing he i s hal o he s udy pe iod.
The obse ed dec ease in synch ony be o e mo ali y ag ees wi h
p e ious s udies in gymnospe ms (Caille e e al., 2019) and is also
consis en wi h he educ ion in g ow h sensi i i y o wa e a ailabili y.
Bo h aspec s indica e a decoupling be ween g ow h and clima ic
luc ua ions, which could be linked o he a o emen ioned less
conse a i e wa e use in dead han in ali e indi iduals (He e o e al.,
2013; p esen s udy), and he subsequen inc ease in ulne abili y o
ca i a ion p ocesses (McDowell e al., 2008). Thus, educ ions in
g ow h synch ony should bealso conside ed as a po en ial indica o
o ee mo ali y isk in seasonally wa e limi ed a eas wi hin
P. syl es is dis ibu ion.
O e all, ou s udy, which akes ad an age o a pai ed design ha
minimizes he e ec s o size and immedia e ee en i onmen on
po en ial causes o mo ali y, highligh s educed sensi i i y o wa e
a ailabili y and g ow h synch ony as po en ial indica o s o d ough -
mo ali y isk in sou he n popula ions o he widely dis ibu ed
P. syl es is. These indica o s could also be ele an o o he isohyd ic
pine species (Salmon e al., 2015) in seasonally d y a eas. Thus,
wesugges he need o assessing changes in g ow h sensi i i y o wa e
a ailabili y in u he s udies (Sua ez e al., 2004; Fé iz e al., 2021;
p esen s udy). Wealso ecommend o u he s udy he esponses o
g ow h sensi i i y o wa e a ailabili y o elucida e he unde lying ee
mo ali y mechanisms a di e en spa ial ex en s and s anda dize he
assessmen me hod o g ow h sensi i i y o wa e a ailabili y, in o de
o make s udies compa able. Despi e ou sampling p o ocol is aimed
o educe en i onmen al di e ences be ween dead and ali e ees,
we canno disca d ha in aspeci ic di e ences be ween ees in
unc ional ai s (e.g., oo ing dep h) and/o in soil p ope ies migh
lead o di e en d ough impac s in sampled ees. In his ega d, he
quan i ica ion o o he a iables, in addi ion o adial g ow h, ela ed
o ee igo (e.g., b anch and olia biomass) and physiological
esponses o d ough (e.g., wa e use e iciency) as well as a mo e obus
e alua ion o compe i ion along ee li espan, may also p o ide aluable
insigh s in o he mechanisms in ol ed in he ee mo ali y p ocess and
in o m o es managemen o he adap a ion o clima e change.
Da a a ailabili y s a emen
The aw da a suppo ing he conclusions o his a icle will
bemade a ailable by he au ho s, wi hou undue ese a ion.
Au ho con ibu ions
EA, PR-B, and AH: sampling design and idea. EA, PG-D, and
PR-B: ield wo k. RG-G: sample p ocessing. EA and AH: analyses. AH:
manusc ip w i ing. All au ho s con ibu ed o he a icle and
app o ed he submi ed e sion.
Funding
AH was suppo ed by he Basque Coun y Go e nmen unding
suppo o FisioKlima-Ag oSosT (IT1682-22) consolida ed esea ch
g oup. EA acknowledges he suppo o g an s PID2019-110470RA-
100 (ADAPTAMIX) unded by MCIN/AEI/10.13039/501100011033,
and REMEDINAL-TE (Communi y o Mad id, S2018/EMT-4338).
PG-D was suppo ed by a pos doc o al con ac unde he g an
RYC2020-029226-I. PR-B and AH we e suppo ed by he Science and
Inno a ion Minis y (subp ojec LARGE, N° _PID2021-123675OB-
C41). PR-B was suppo ed by he Communi y o Mad id Region unde
he amewo k o he mul i-yea Ag eemen wi h he Uni e si y o
Alcalá (S imulus o Excellence o Pe manen Uni e si y P o esso s,
EPU-INV/2020/010).
Acknowledgmen s
We hank Daniel Gómez and Pablo Quiles o ield assis ance.
FIGURE5
Tempo al e olu ion o g ow h synch ony es ima es (âc) o li e and
dead ees o he 1948–2017 s udy pe iod. Da a a e showed o
20-yea in e als wi h a 5-yea s mo ing window. The yea s
appea ing on he x-axis co espond o he midpoin s o each 20-
yea in e al.
He e o e al. 10.3389/ gc.2023.1249246
F on ie s in Fo es s and Global Change 08 on ie sin.o g
Con lic o in e es
The au ho s decla e ha he esea ch was conduc ed in he
absence o any comme cial o inancial ela ionships ha could
becons ued as a po en ial con lic o in e es .
Publishe ’s no e
All claims exp essed in his a icle a e solely hose o he au ho s
and do no necessa ily ep esen hose o hei a ilia ed
o ganiza ions, o hose o he publishe , he edi o s and he
e iewe s. Any p oduc ha may be e alua ed in his a icle, o
claim ha may be made by i s manu ac u e , is no gua an eed o
endo sed by he publishe .
Supplemen a y ma e ial
The Supplemen a y ma e ial o his a icle can be ound online
a : h ps://www. on ie sin.o g/a icles/10.3389/ gc.2023.1249246/
ull#supplemen a y-ma e ial
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