A e pine-oak mixed s ands in Medi e anean moun ains mo e esilien
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o d ough han hei monospeci ic coun e pa s?
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F ancisco Muñoz-Gál ez1, Asie He e o2, Es he Pé ez-Co ona3, En ique Andi ia3
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1 Te es ial Ecosys em Ecology and Conse a ion Resea ch G oup, Depa men o
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Ecology, Uni e sidad Au ónoma de Mad id, Mad id, Spain.
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2 Fo es Ecology and Res o a ion G oup, Depa men o Li e Sciences, Uni e si y o
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Alcala, Alcalá de Hena es, Spain.
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3 Depa men o Biodi e si y, Ecology and E olu ion, Uni e sidad Complu ense de
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Mad id, Mad id, Spain.
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This is he accep ed manusc ip o he a icle ha appea ed in inal o m in Fo es Ecology and Managemen 484: (2021) //
A icle ID 118955, which has been published in inal o m a h ps://doi.o g/10.1016/j. o eco.2021.118955. © 2021 Else ie unde
CC BY-NC-ND license (h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/)
Abs ac
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Clima e change p ojec ions poin o an inc ease in he in ensi y and equency o ex eme
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d ough e en s wi h impo an nega i e impac s on o es unc ioning. P edic ing hese
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impac s cons i u es a c ucial challenge o o es manage s and o he main enance o
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ecosys em se ices supply. P omo ing mixed s ands seems a p omising s a egy o
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adap ing o es ecosys ems o ongoing clima e change. Howe e , some unce ain y exis s
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ega ding whe he mixed s ands can imp o e g ow h esilience o ex eme d ough e en s.
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He e, we aim o assess ee g ow h esponse o d ough in mixed and monospeci ic s ands
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o Pinus syl es is L. and Que cus py enaica Willd. in cen al Spain. We buil ee- ing
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ch onologies, and e alua ed ee g ow h sensi i i y o wa e a ailabili y and g ow h
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esilience componen s o ex eme d ough s using linea mixed models. We ound
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con as ing species- and clima e-speci ic esponses o admix u e. Q. py enaica g ow h
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was signi ican ly highe in mixed han in monospeci ic s ands in yea s wi hou wa e
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limi a ions, while P. syl es is showed highe g ow h in mixed s ands unde d y
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condi ions. Consequen ly, P. syl es is and Q. py enaica showed highe esis ance and
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eco e y o d ough in mixed han monospeci ic s ands, espec i ely. Howe e , Q.
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py enaica was mo e esis an in monospeci ic han mixed s ands. Ou esul s highligh
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he impo ance o wa e a ailabili y and species-speci ic esponses when e alua ing
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admix u e e ec s on d ough ulne abili y. O e all, we show posi i e e ec s o
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admix u e on ee g ow h and esilience componen s o bo h P. syl es is and Q.
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py enaica, suppo ing admix u e as a managemen op ion o adap a ion o Medi e anean
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moun ain o es s o clima e change.
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Keywo ds: Clima e change, complemen a i y, o es managemen , g ow h s abili y,
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Pinus syl es is, Que cus py enaica, ee di e si y.
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1. In oduc ion
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Clima e change is globally al e ing o es composi ion, s uc u e and unc ioning
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(Allen e al., 2010, 2015; Ruiz-Beni o e al., 2017), which ul ima ely comp omises he
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p o ision o key ecosys em se ices o human well-being (Nelson e al., 2013).
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Medi e anean o es s can be especially ulne able ecosys ems due o i s high exposi ion
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o clima e change (Lindne e al., 2010). O e he las cen u y, empe a u e inc eased in
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he Medi e anean basin by 1.4 ºC (C ame e al., 2018), exace ba ing d ough impac s on
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ee g ow h and igge ing d ough -induced mo ali y e en s (G eenwood e al., 2017;
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Gazol e al., 2018; Mad igal-González e al., 2018). Clima e change scena ios p ojec a
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wo isome inc ease o 2-5 ºC along 21s cen u y coupled wi h a dec ease in p ecipi a ion
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o up o 30%, and a highe equency and in ensi y o ex eme d ough e en s (IPCC,
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2018; Spinoni e al., 2018). Thus, he e is an u gen need o imp o e ou knowledge abou
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o es esponse o ex eme d ough s and o adequa e managemen s a egies o enhance
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long- e m o es esilience.
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Admix u e, i.e. he inc ease in ee species di e si y, may con ibu e o s abilize
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o es unc ioning and ecosys em se ices supply in esponse o dis u bances (Gam eld
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e al., 2013). Se e al s udies ha e showed a posi i e ela ionship be ween ee di e si y
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and o es p oduc i i y a di e en spa ial scales (Paque e and Messie , 2010; Ruiz-
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Beni o e al., 2014; P e zsch e al., 2015, 2019; Liang e al., 2016; Jac el e al., 2018).
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Admix u e can also s abilize o es p oduc i i y and educe g ow h sensi i i y o clima ic
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a iabili y (del Río e al., 2017). All his body o e idence has led o he p omo ion o
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mixed s ands in o es y p ac ice wo ldwide (Bol e e al., 2010). Howe e , some s udies
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ha e epo ed a dec ease in he magni ude o he posi i e e ec o ee di e si y on o es
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p oduc i i y wi h d ough s ess (Jac el e al., 2018; Toïgo e al., 2015). Fu he mo e,
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he e is some unce ain y ega ding admix u e e ec s on he s abili y o o es
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p oduc i i y o ex eme d ough e en s (G ossio d, 2019). In his ega d, g ow h
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esilience, i.e. he capaci y o indi iduals o es o e p e-dis u bance g ow h a es a e a
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dis u bance (Holling, 1996; Llo e e al., 2011), is an inc easingly adop ed concep o
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e alua e o es s abili y o ex eme d ough s (Nikinmaa e al., 2020). Despi e some
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e idence o posi i e e ec s o admix u e on esilience o d ough (Lebou geois e al.,
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2013; Gazol and Cama e o, 2016; S eckel e al., 2020), o he s udies epo ed species- o
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si e-speci ic e ec s (P e zsch e al., 2013; G ossio d e al., 2014; Mölde and Leuschne ,
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2014; Me lin e al., 2015; G anda e al., 2018; Jou dan e al., 2019a, 2019b). In addi ion,
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ew s udies ha e been conduc ed in Medi e anean a eas (G anda e al., 2018), hampe ing
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ou abili y o make a co ec assessmen o admix u e as an app op ia e managemen
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op ion o adap a ion o Medi e anean o es s o clima e change.
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Admix u e posi i e e ec s on o es p oduc i i y a e commonly in e p e ed on he
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basis o complemen a i y, which includes bo h compe i ion educ ion and acili a ion
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mechanisms (Amme , 2019). On one hand, compe i ion educ ion usually occu s h ough
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niche pa i ioning, due o in e -speci ic di e ences in physiology, mo phology and
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phenology, leading o dispa a e esou ce acquisi ion s a egies (Fo es e , 2014; Fo es e
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and Bauhus, 2016). On he o he hand, acili a ion implies ha one species inc eases he
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pe o mance o coexis ing species (Callaway, 1995). Ac i e hyd aulic edis ibu ion
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(Que eje a e al., 2003; Zapa e e al., 2011) and noc u nal wa e elease (P ie o e al.,
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2012) a e examples o acili a i e mechanisms ha esul in inc eased soil mois u e.
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These complemen a i y e ec s ha e been also associa ed wi h he biodi e si y-s abili y
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ela ionship (Lo eau and de Mazancou , 2013), al hough o he mechanisms such as
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empo al shi s in species in e ac ions (del Río e al., 2017) and asynch onic species-
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speci ic esponses o en i onmen al luc ua ions (Mo in e al., 2014) ha e been also
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p oposed.
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Mos o he esea ch on complemen a i y e ec s on o es ecosys ems ha e been
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conduc ed in o es s wi hou se e e wa e limi a ions, whe e ligh - ela ed in e ac ions
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d i e complemen a i y e ec s (e.g. Baye e al., 2013; P e zsch, 2014; Fo es e and
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Bauhus, 2016). In seasonally d y a eas, such as he Medi e anean basin, admix u e
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posi i e e ec s ely on educing compe i ion o wa e and/o imp o ing wa e
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a ailabili y (Jucke e al., 2014; Ruiz-Beni o e al., 2014). Medi e anean ee species
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show a wide a ie y o wa e use s a egies associa ed wi h di e en s uc u al and
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physiological adap a ions, such as s oma al beha iou (isohyd ic s. anisohyd ic species)
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and oo ing s a egy ( ap oo s supe icial) (Za ala e al., 2000; Mo eno-Gu ié ez e al.,
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2012; del Cas illo e al., 2016; Ma ín-Gómez e al., 2017). This sugges s he exis ence o
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complemen a i y mechanisms among species ha would educe compe i ion o wa e in
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mixed o es s and hus, enhance esilience o ex eme d ough s. Howe e , whe he
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admix u e modi ies ee esponses o d ough compa ed o monospeci ic s ands is s ill
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unde deba e (G ossio d, 2019).
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Medi e anean Ibe ian o es s a e excellen models o he e alua ion o admix u e
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e ec s on d ough impac s (Vilà-Cab e a e al., 2018). Many o he cu en coni e ous
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o es s o he Ibe ian Peninsula (mainly Pinus spp.) a e he esul o la ge-scale
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a o es a ion policies du ing he 20 h cen u y (Vadell e al., 2016). The lack o subsequen
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o es managemen has esul ed in s uc u ally and unc ionally homogeneous e en-aged
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dense s ands (Villa -Sal ado , 2016), which o en show low g ow h a es (Gómez-
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Apa icio e al., 2009), high mo ali y (Sánchez-Salgue o e al., 2012), lack o egene a ion
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(Ruiz-Beni o e al., 2012), and high ulne abili y o i es and pes s (Maes e and Co ina,
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2004). In his con ex , he admix u e o oaks (Que cus spp.) in pine monospeci ic s ands
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can be conside ed as a powe ul ool o manage Medi e anean o es s in he ace o
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clima e change (Pausas e al., 2004), by bo h sp eading d ough -impac isk among
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mul iple species and bene icial complemen a i y e ec s.
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In his s udy, we compa ed ee g ow h esponse o d ough condi ions in mixed
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and monospeci ic s ands o Sco s pine (Pinus syl es is L.) and Py enean oak (Que cus
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py enaica Willd.) in cen al Spain. These species a e equen ly mixed in ex ensi e a eas
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o Ibe ian moun ains a he eco one be ween monospeci ic pine and oak s ands (Sánchez
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de Dios e al., 2019). We employed a s and-le el “ iple design” coupled wi h ee- ing
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da a o analyze he e ec o wa e a ailabili y on ee g ow h a an annual scale in bo h
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monospeci ic and mixed s ands. Following his app oach, we also quan i ied g ow h
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esilience, and associa ed componen s ( esis ance and eco e y), o ex eme d ough
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e en s occu ed du ing he las decades using he indices p oposed by Llo e e al. (2011).
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Due o unc ional di e ences be ween a ge species ega ding shade ole ance, lea habi ,
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oo ing dep h and wa e use s a egies (del Cas illo e al., 2016; Ma ín-Gómez e al.,
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2017; Mo eno-Gu ié ez e al., 2012), we hypo hesized lowe d ough -induced g ow h
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educ ions and highe esilience o ex eme d ough s in mixed han monospeci ic s ands
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due o complemen a i y e ec s.
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2. MATERIAL AND METHODS
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2.1. S udy a ea
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The s udy was conduc ed in he Sie a de Guada ama Na ional Pa k, in he cen e
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o he Ibe ian Peninsula (40º 50’ 26’’ N; 3º 49’ 34’’ W). Clima e is con inen al
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Medi e anean, cha ac e ized by cold win e s and wa m and d y summe s, wi h
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p ecipi a ions concen a ed in au umn and sp ing. Mean annual empe a u e and o al
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p ecipi a ion is 11.4ºC and 555.7 mm, espec i ely (pe iod 1961-2018; da a om CRU
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TS3.10 da abase, Ha is e al. (2014)). P. syl es is is he dominan ee species a high
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al i ude, co-occu ing wi h Q. py enaica a in e media e al i ude (1,200-1,600 m a.s.l.),
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al hough he la e can also be ound o ming ex ensi e monospeci ic s ands. Unde s o y
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species a y wi h al i ude, being P e idium aquilinum ((L.) Kuhn), Genis a lo ida (L.),
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Ilex aqui olium (L.) and C a aegus monogyna (Jacq.) he mos ep esen a i e species.
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2.2. Sampling design
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We selec ed six independen o es si es on he sou he n ace o he Sie a de
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Guada ama a an al i ude ha anged om 1,286 o 1,544 m a.s.l. (Table 1). A each si e
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we selec ed 15 s ands o 20 x 20 m (0.04 ha) ollowing a iple design. Thus, we sampled
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i e monospeci ic s ands o each species (100% o he basal a ea) and i e mixed s ands
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(basal a ea o he dominan ee species was lowe han 70%). Field sampling was ca ied
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ou om No embe 2018 o Feb ua y 2019. We selec ed one ee in each monospeci ic
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s and and wo ees (one o each species) in mixed s ands (he eina e ocal ees). Focal
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ees we e selec ed in he cen e o he s and, and hey we e all dominan o co-dominan
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wi h no sign o igou decline (i.e. de olia ion o d y b anches) o physical damages (e.g.
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due o snow o he bi o y). In mixed s ands, he dis ance be ween ocal ees was lowe
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han 5 m. We eco ded he diame e a b eas heigh (DBH) o each a ge ee and each
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neighbo ing ee wi hin a ci cula plo o 7 m adius measu ed om he ocal ee. We
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calcula ed he basal a ea o he ci cula plo and he Lo ime ’s dis ance-independen
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compe i ion index (LCI) (Lo ime , 1983) as:
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𝐿𝐶𝐼%=
'
𝐷𝐵𝐻+𝐷𝐵𝐻%
⁄
-
+./
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whe e DBHi is he diame e a b eas heigh o he a ge ee i, and DBHj is he diame e
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a b eas heigh o he neighbo ing ee j.
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2.3. Dend oecological me hods
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We ex ac ed one wood co e pe a ge ee a b eas heigh using a P essle
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inc emen bo e (5 mm; Haglö , Sweden). Wood co es we e p ocessed ollowing s anda d
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dend och onological me hods (F i s, 1976). Fi s , wood co es we e ai -d ied and glued
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on wooden suppo s. Then, hey we e sanded using sandpape s o p og essi ely ine
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g ains o maximize he isibili y o he ee ings. T ee g ow h se ies we e isually c oss-
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da ed using poin e yea s (Yamaguchi, 1991). Wood co es we e scanned a 1,200 dpi
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esolu ion (EPSON® Pe ec ion 800) and ee- ing wid hs we e measu ed o he nea es
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0.01 mm using ImageJ® (Schneide e al., 2012).
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Ring-wid h se ies we e con e ed o basal a ea inc emen (BAI) assuming s em
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g ow h is app oxima ely concen ic:
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𝐵𝐴𝐼 =1𝜋(𝑟56−1𝑟58/6)
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whe e and -1 a e he s em adius a he end and a he beginning o a gi en annual ing,
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espec i ely. BAI e lec s whole ee g ow h be e han he one-dimensional g ow h o
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ee ing wid h (Biondi and Qeadan, 2008). We also quan i ied annual ee size as he
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basal a ea o he ee o he whole BAI se ies, ep esen ing he inc ease in size wi h
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ageing. E en hough he oldes ee was da ed o 1905, we selec ed as s udy pe iod 1961-
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2018 o he obus ness o s a is ical analysis (70% o he a ge ees in 1961).
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2.4. Iden i ica ion o ex eme d ough e en s
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We used he CRU TS3.10 da abase (Ha is e al., 2014) o cha ac e ized he
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clima e o he s udy si es o he pe iod 1961-2018. Annual mean empe a u e and annual
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p ecipi a ion om his da abase we e highly co ela ed ( = 0.89 and 0.74, espec i ely
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using common yea s) wi h da a om he nea es me eo ological s a ion (Na ace ada, 25
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km a om he closes si e and a 1,894 m a.s.l). Wa e a ailabili y (P-PET) was
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cha ac e ized as he di e ence be ween annual p ecipi a ion and po en ial
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e apo anspi a ion (PET) ollowing Bigle e al. (2006). PET was calcula ed ollowing
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Tho n hwai e (1948). We calcula ed P-PET om Oc obe o he p e ious yea o
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Sep embe o he p esen yea o accoun o he in luence o p e ious yea condi ions on
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he cu en g owing season (Mad igal-González e al., 2017a).
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D ough e en s we e iden i ied as ex emely d y yea s wi h a signi ican educ ion
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on ee g ow h (Schweing ube e al., 1990). Speci ically, we selec ed as ex eme
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d ough s hose yea s whe e P-PET was below he 15 h pe cen ile o he ime se ies (i.e. P-
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PET alues unde -251.4 mm) and whe e a leas 60% o he sampled ees showed a BAI
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educ ion o a leas 20% ela i e o he BAI a e age in he h ee p eceding yea s. We
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selec ed 1986, 1995, 2005, 2012 and 2017 as ex eme d ough e en s (Fig. S1).
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2.5. Resis ance, esilience and eco e y o d ough e en s
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To e alua e g ow h esponses o selec ed d ough e en s, we calcula ed g ow h
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esis ance, esilience and eco e y indices ollowing Llo e e al. (2011):
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𝑅𝑒𝑠𝑖𝑠𝑡𝑎𝑛𝑐𝑒1 =1𝐷𝑟 𝑃𝑟𝑒𝐷𝑟
⁄
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𝑅𝑒𝑠𝑖𝑙𝑖𝑒𝑛𝑐𝑒1 =1𝑃𝑜𝑠𝑡𝐷𝑟 𝑃𝑟𝑒𝐷𝑟
⁄
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𝑅𝑒𝑐𝑜𝑣𝑒𝑟𝑦1=1𝑃𝑜𝑠𝑡𝐷𝑟 𝐷𝑟
⁄
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whe e D is he BAI he yea o he d ough e en and P eD and Pos D he mean BAI
196
o h ee yea s be o e and a e he d ough e en , espec i ely. We only calcula ed
197
esis ance index in 2017 since g ow h se ies inished in 2018. We also cha ac e ized wa e
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a ailabili y di e ences be ween e alua ed pe iods as:
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𝑃𝑃𝐸𝑇IJK%K5L-MJ 1=1𝑃𝑃𝐸𝑇NI −𝑃𝑟𝑒𝑃𝑃𝐸𝑇
200
𝑃𝑃𝐸𝑇IJK%O%J-MJ 1= 1𝑃𝑜𝑠𝑡𝑃𝑃𝐸𝑇−𝑃𝑟𝑒𝑃𝑃𝐸𝑇
201
± 0.04, espec i ely), whe eas P. syl es is showed simila eco e y in bo h s and ypes
297
(1.28 ± 0.04 and 1.39 ± 0.04) (Fig. 3b, Table S5). In addi ion, g ow h eco e y was also
298
a ec ed by di e ences in wa e a ailabili y a e d ough (P-PET ec) and by he
299
in e ac ion species × d ough in ensi y (P-PETd ). Bo h species showed g ea e eco e y
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wi h inc easing P-PET ec and dec easing P-PETd , espec i ely (Table S6). Howe e , he
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inc ease in eco e y wi h dec easing d ough in ensi y was highe in Q. py enaica han in
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P. syl es is (es ima ed model slopes ± SE, 0.35 ± 0.05 and 0.14 ± 0.05, espec i ely; Fig
303
4a, Table S6).
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G ow h esilience was also a ec ed by wa e a ailabili y di e ences be ween he
305
pos - and he p e-d ough pe iods (P-PET es) and by he in e ac ion species × d ough
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in ensi y (P-PETd ) (Table S7). Howe e , we did no ind any e ec o s and ype on
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g ow h esilience (Fig. 3c). G ow h esilience was nega i ely ela ed o P-PET es
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(es ima ed model slope ± SE, -0.20 ± 0.06). Analogously o g ow h eco e y, esilience
309
inc eased wi h dec easing d ough in ensi y, especially in Q. py enaica (es ima ed model
310
slopes ± SE, 0.46 ± 0.06 and 0.002 ± 0.06, espec i ely) (Fig 4b). G ow h esilience was
311
also a ec ed by he in e ac ion species × ee size. G ow h esilience dec eased wi h ee
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size in P. syl es is, bu no e ec was ound in Q. py enaica (es ima ed model slopes ±
313
SE, 0.07 ± 0.02 and 0.02 ± 0.02, espec i ely; Table S8).
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315
Figu e 3: Boxplo s o g ow h esis ance (a), eco e y (b) and esilience (c) o s udy
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species and s and ype. Fo each boxplo , he P- alue o he compa ison be ween s and
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ypes is showed. As e isks show signi ican in e ac ions (P < 0.05). Boxes a e 95% and
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5% pe cen ile alues, whiske s depic maximum and minimum alues and he solid lines
319
indica e he median.
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321
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Figu e 4: Model p edic ion (± 95% con idence in e al) o g ow h eco e y (a) and
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esilience (b) o each s udy species in esponse o d ough in ensi y (P-PETd ).
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325
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4. DISCUSSION
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4.1. Admix u e e ec s on ee g ow h and esilience componen s
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Ou esul s show bene icial e ec s o admix u e on ee g ow h o he widely dis ibu ed
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sub-Medi e anean Q. py enaica and bo eal P. syl es is in d ough -limi ed
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Medi e anean moun ains. Admix u e posi i e e ec s on ee g ow h esponse o wa e
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a ailabili y we e species-speci ic, which esul ed in con as ing e ec s on he di e en
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componen s o g ow h esilience o ex eme d ough e en s. P. syl es is showed highe
333
g ow h in mixed han in monospeci ic s ands in yea s wi h low wa e a ailabili y, which
334
also esul ed in a highe g ow h esis ance o ex eme d ough s in mixed s ands. On he
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con a y, g ow h di e ences be ween mixed and monospeci ic s ands inc eased wi h
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inc easing wa e a ailabili y o Q. py enaica, showing highe eco e y a e ex eme
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d ough e en s in mixed s ands. On he one hand, hese esul s can help o cla i y he
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ongoing deba e on he ela ionship be ween ee di e si y and esilience o d ough in
339
o es ecosys ems, poin ing o he impo ance o species- and clima e-speci ic e ec s. On
340
he o he hand, ou esul s ha e key implica ions o o es managemen , sugges ing
341
P.syl es is-Q. py enaica mixed s ands as an adap a ion solu ion o mid-ele a ion o es s
342
in he Ibe ian Peninsula unde inc eased a idi y.
343
The posi i e e ec o admix u e on ee g ow h can be explained by
344
complemen a i y due o bo h mechanisms, acili a ion and compe i ion educ ion (Lo eau
345
and Hec o ., 2001; Callaway, 2007; B ooke e al., 2008). Acco ding o he s ess g adien
346
hypo hesis (Be ness and Callaway, 1994), posi i e in e ac ions among species a e mo e
347
common in a eas wi h high en i onmen al s ess, which is he case o d ough -limi ed
348
o es s in Medi e anean moun ains (e.g. Gómez-Apa icio e al., 2004). On he one hand,
349
compe i ion educ ion elies on in e -speci ic di e ences in esou ce acquisi ion
350
s a egies. S udy species show ema kable di e ences in shade ole ance, lea phenology,
351
wa e -use s a egy, and oo s uc u e (Niineme s and Vallada es, 2006; Poya os e al.,
352
2008; Río and S e ba, 2009). Among hem, e ical oo ing s a i ica ion is a key
353
complemen a i y mechanism in d ough -limi ed o es ecosys ems (G ossio d, 2019). In
354
his ega d, some s udies in mixed s ands showed ha coni e s ha e access o shallowe
355
wa e esou ces while oak species can access deepe ones due o a mo e ex ensi e and
356
deep oo sys em (Poya os e al., 2008; del Cas illo e al., 2016; Ma ín-Gómez e al.,
357
2017). On he o he hand, acili a ion could occu h ough hyd aulic li by oak species
358
unde mode a e and se e e d ough condi ions, which inc eases wa e a ailabili y in he
359
uppe soil ho izons o he admixed species (Que eje a e al., 2003; Zapa e e al., 2011).
360
The highe g ow h du ing d y yea s and esis ance o ex eme d ough s o P.
361
syl es is in mixed han monospeci ic s ands migh be d i en mainly by wa e - ela ed
362
acili a ion mechanisms. Hyd aulic li can inc ease no only wa e a ailabili y o P.
363
syl es is, bu also oo g ow h and unc ioning as well as nu ien a ailabili y due o
364
posi i e e ec s o inc easing humidi y on o ganic ma e decomposi ion and
365
mine aliza ion (Ro he and Binkley, 2001; Richa ds e al., 2010; P ie o e al., 2012, del
366
Cas illo e al., 2016). Compe i ion educ ion in esponse o low wa e a ailabili y seems
367
no o play a p e ailing ole in ou s udy since admix u e showed neu al e ec s on Q.
368
py enaica g ow h in d y yea s. In ac , Q. py enaica showed highe esis ance o ex eme
369
d ough s in monospeci ic han in mixed s ands. Acco dingly, S eckel e al., (2020)
370
showed a educ ion o admix u e posi i e e ec s on Q. obu and Q. pe aea esponse o
371
d ough in d ies si es when co-occu ing wi h P. syl es is.
372
In e es ingly, admix u e posi i e e ec s on Q. py enaica g ow h eme ged wi h
373
inc easing wa e a ailabili y. Reduced in e -speci ic compe i ion coupled o highe
374
abo e- and below-g ound compe i i e capaci y could allow Q. py enaica o maximize
375
ligh and nu ien cap u e in mixed s ands unde non-limi ed wa e condi ions
376
(Longue aud e al., 2013; Mad igal-González e al., 2016), which migh also explain he
377
highe eco e y o Q. py enaica a e ex eme d ough s in mixed han in monospeci ic
378
s ands. In addi ion, unc ional di e ences in lea ai s be ween s udy species can also
379
imp o e mine aliza ion and decomposi ion p ocesses, ul ima ely inc easing nu ien
380
a ailabili y in mixed s ands (Ro he and Binkley, 2001; Andi ia e al., 2016; San onja e
381
al., 2017). Despi e P. syl es is is also likely o bene i om inc eased nu ien
382
a ailabili y, compe i ion o ligh could o se posi i e admix u e e ec s unde mode a e
383
o high wa e a ailiabili y condi ions due o la ge lea a eas. In his con ex , Q. py enaica
384
could be a ou ed o e P. syl es is due o i s b oad-lea ed habi and highe ole ance o
385
shade (Za ala e al., 2000; Niineme s and Vallada es, 2006).
386
4.2. G ow h esilience componen s
387
To analyze g ow h esilience componen s, we simul aneously conside ed all ex eme
388
d ough e en s occu ed du ing ecen decades (1986-2018), which ep esen s a mo e
389
ealis ic app oach o assess o e all g ow h esponse o d ough han analyzing each e en
390
sepa a ely. In ac , unde ongoing clima e change, ees a e exposed o ecu en ex eme
391
d ough e en s (Spinoni e al., 2018), which has been p o ed o educe he esilience
392
capaci y o o es ee species (Andi ia e al., 2020; Se a-Maluque e al., 2018).
393
Howe e , by doing so, we did no accoun o speci ic de ails abou d ough onse and
394
du a ion o each e en , which could in luence species d ough sensi i i y (Ho mann e
395
al., 2018). To pa ly a oid his, we ollowed ecen ecommenda ions o quan i y g ow h
396
esilience (DeSo o e al., 2020; Schwa z e al., 2020). Speci ically, we e alua ed g ow h
397
esilience componen s a e con olling o among-e en s di e ences in d ough in ensi y
398
(PPETd ) and wa e a ailabili y di e ences be ween g ow h pe iods (PPET e, PPET es,
399
PPET ec).
400
Dec easing d ough in ensi y and di e ences in wa e a ailabili y be ween pos -
401
and d ough pe iods had a posi i e e ec on g ow h eco e y o bo h species. This ag ees
402
wi h o he s udies poin ing o he impo ance o si e clima ic condi ions on g ow h
403
eco e y capaci y (Gazol e al., 2017; S eckel e al., 2020). Dec easing d ough in ensi y
404
also inc eased esilience o Q. py enaica, bu no o P. syl es is. This, and he highe
405
e ec o dec easing d ough in ensi y on Q. py enaica eco e y, migh be pa ly explained
406
by he anisohyd ic beha io o oaks, i.e. he p ese a ion o anspi a ion a es a low
407
wa e po en ial (Fe nández-De-Uña e al. 2017, Ma ín-Gómez e al. 2017). Thus, Q.
408
py enaica migh ake ad an age o inc eased wa e a ailabili y, and as e e illing o soil
409
wa e ese es wi h dec easing d ough in ensi y, o maximize pos -d ough ee g ow h,
410
and hus eco e y and esilience. In ac , oak species a d y si es show posi i e d ough
411
legacies (Ande egg e al., 2015). On he con a y, he isohyd ic beha io o P. syl es is
412
(i.e. igh s oma al con ol unde d ough condi ions; I ine e al., 1998), seems o espond
413
o speci ic d ough h eshold h ough p olonged s oma a closu e, educing pho osyn hesis
414
and deple ing ca bohyd a e ese es, which migh ul ima ely impai pos -d ough g ow h.
415
Finally, he nega i e e ec o di e ences in wa e a ailabili y be ween pos - and p e-
416
d ough pe iods on esilience may e lec a nega i e legacy o mode a e d y condi ions
417
du ing p e-dis u bance pe iod on pos -d ough g ow h. We also conside ed ee size when
418
e alua ing g ow h esilience componen s, since size s ongly in luences ee g ow h
419
dynamics and hus esilience capaci y (Andi ia e al., 2020). T ee size was nega i ely
420
ela ed o g ow h esilience o P. syl es is, which con as s o p e ious s udies wi h his
421
species using di e en size ca ego ies (Me lin e al., 2015). La ge ees can be mo e
422
exposed o d ough due o hei g ea e olia biomass and he dominan posi ion in he
423
s and (Ma ín-Beni o e al., 2008), which migh inc ease wa e demand and espi a ion
424
cos s a ec ing pos -d ough eco e y.
425
Con a y o ou hypo hesis, we did no ind di e ences in species esilience
426
capaci y media ed by s and ype. These esul s can be ela ed o epo ed ade-o s
427
be ween g ow h esis ance and eco e y (Hodgson e al., 2015; Ho mann e al., 2018).
428
This ade-o migh explain he obse ed highe eco e y in mixed s ands and highe
429
esis ance in monospeci ic ones o Q. py enaica. The lack o his ade-o o P.
430
syl es is, which showed highe esis ance in mixed han monospeci ic s ands bu simila
431
eco e y, could be due o he abo e-men ioned s ong nega i e d ough legacy e ec s
432
epo ed o coni e species (Ande egg e al., 2015), which could impai pos -d ough
433
eco e y in bo h ype o s ands.
434
4.3. Implica ions o o es managemen
435
Ou esul s showed posi i e e ec s o admix u e on ee g ow h and esilience
436
componen s o bo h P. syl es is and Q. py enaica. The posi i e e ec o admix u e on
437
P. syl es is g ow h esponse du ing d y yea s and esis ance o ex eme d ough s can be
438
c i ical a he sou he n dis ibu ion limi o he species unde inc eased a idi y condi ions.
439
In addi ion, enhancemen o Q. py enaica ee g ow h in yea s wi hou wa e limi a ions,
440
sugges s ha inc easing ee di e si y can also con ibu e o inc ease he p oduc i i y o
441
Medi e anean moun ain o es s (Río and S e ba, 2009). On he o he hand, we ound a
442
nega i e e ec o compe i ion on ee g ow h i espec i ely o species iden i y and he
443
ype o s and analysed, which sugges s ha hinning is a key ool o imp o e o es
444
esilience and esponse o d ough , in ag eemen wi h p e ious s udies (Kohle e al.,
445
2010; Sohn e al. 2016). This is especially ele an o monospeci ic coni e s ands in he
446
Ibe ian peninsula, since lack o o es managemen du ing he las decades ha e led o
447
dense s ands wi h a high ulne abili y o d ough , i es and pes s (Maes e and Co ina,
448
2004; Gómez-Apa icio e al., 2011; Sánchez-Salgue o e al., 2012). Howe e , d ough
449
impac s on o es dynamics ely no only on ee g ow h esponses bu also on ec ui men
450
and mo ali y (Allen e al., 2010; Mad igal-González e al., 2017b). Thus, u he s udies
451
should also e alua e admix u e e ec s on o he demog aphic a es o p o ide a
452
comp ehensi e iew o he esponse o mixed s and o d ough e en s (Andi ia e al.,
453
2020; Mad igal-González e al., 2017b). This is o pi o al impo ance o p ope ly e alua e
454
ee di e si y e ec s on o es esilience, bu also o design o es managemen s a egies
455
o ien ed o gua an ee he long- e m pe sis ence o mixed s ands.
456
457
5. CONCLUSIONS
458
Ou esul s sugges ha mixed s ands o P. syl es is and Q. py enaica a e less ulne able
459
o d ough han hei monospeci ic coun e pa s, co obo a ing posi i e complemen a i y
460
e ec s be ween con as ing unc ional species. Thus, his s udy con ibu es o he g owing
461
body o e idences suppo ing admix u e as a managemen op ion o adap a ion o o es s
462
o clima e change. P omo ing mixed s ands o pine and oak species may con ibu e o
463
inc ease o es p oduc i i y while educing ulne abili y o clima ic dis u bances.
464
Howe e , posi i e e ec s on ee g ow h and esilience we e species-speci ic and
465
con ingen upon wa e a ailabili y, which sugges s ha u he s udies should include
466
mo e species combina ion and he whole en i onmen al g adien o e he na u al a ea
467
whe e species co-occu .
468
469
Acknowledgemen s
470
We acknowledge unding suppo by ADAPTAMIX (Spanish Minis y o Science and
471
Inno a ion, PID2019-110470RA-I00) and REMEDINAL-TE (Regional Go e nmen o
472
Mad id, S2018/EMT-4338) g an s, and by Complu ense Uni e si y o Mad id and Banco
473
San ande (GR105/18). EA was suppo ed by a Pos doc o al g an unded by he
474
Complu ense Uni e si y o Mad id (CT39/17) and AH by he Uni e si y o Alcalá Own
475
Resea ch P og amme’s 2019/20 Pos doc o al G an . We hank Raquel González, Julen
476
As iga aga and E a Monse a o hei help du ing ield wo k.
477
478
Decla a ion o in e es s: None
479
480
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