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European Journal of Forest Research ISSN 1612-4669 Eur J Forest ResDOI 10.1007/s10342-013-0768-0

Effects of past growth trends and currentwater use strategies on Scots pine andpubescent oak drought sensitivity

T. Morán-López, R. Poyatos, P. Llorens& S. Sabaté

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ORIGINAL PAPER

Effects of past growth trends and current water use strategieson Scots pine and pubescent oak drought sensitivity

T. Moran-Lopez • R. Poyatos • P. Llorens •

S. Sabate

Received: 19 June 2013 / Revised: 26 November 2013 / Accepted: 6 December 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract Drought-induced decline is affecting Pinus syl-

vestris populations in southern Europe, with very little

impact on the more drought-tolerant Quercus pubescens.

Although multiple studies have investigated interspecific

differences in water use and growth strategies, the link

between these two processes and how they vary within

drought-exposed populations remains poorly understood.

Here, we analysed tree ring and sap flow data from P. syl-

vestris and Q. pubescens stands in the Pyrenees in order to

(1) evaluate differences in climate–growth responses among

species, (2) disentangle the role of past growth trends and

water use strategies in individual trees drought sensitivity

and (3) assess whether such intraspecific patterns vary

between species. Both species have suffered recent climatic

constraints related to increased aridity. However, the effects

of past growth trends and current water use traits on drought

sensitivity varied among them. Initially, fast-growing

‘drought-sensitive’ pines displayed a higher gas exchange

potential but were more sensitive to evaporative demand and

soil moisture. They also showed lower water use efficiency

for growth (WUEBAI) and current growth decline. In con-

trast, initially, slow-growing ‘drought-tolerant’ pines

showed the opposite water use traits and currently maintain

the highest growth rates. In comparison, neither current

WUEBAI nor recent growth trends varied across Q. pubes-

cens climate–growth groups. Nonetheless, ‘drought-sensi-

tive’ oaks showed the lowest gas exchange potential and the

highest growth rates under milder conditions. Our results

show a strong effect of past growth trends and current water

use strategies on tree resilience to increased aridity, which is

more evident in P. sylvestris.

Keywords Climate–growth relationships � Drought-

induced decline � Pinus sylvestris � Quercus pubescens �Sap flow � Water use efficiency (WUE)

Introduction

Climate change projections predict a general increment in

mean temperatures as well as changes in the seasonal dis-

tribution of precipitation in the Mediterranean basin (IPCC

2007). In the case of the Iberian Peninsula, a general trend

of temperature increments between 3 and 4 �C on average

accompanied by reduced precipitations from 10 to 25 % is

expected by the end of the century (Christensen and

Christensen 2007). Particularly, throughout the Pyrenees,

symptoms of more intense summer droughts and lower

winter precipitations have already been observed, and

enhanced water shortage is expected towards the end of the

present century (Lopez-Moreno and Nogues-Bravo 2005).

Communicated by R. Matyssek.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10342-013-0768-0) contains supplementarymaterial, which is available to authorized users.

T. Moran-Lopez (&) � S. Sabate

Department of Ecology, University of Barcelona,

08028 Barcelona, Spain

e-mail: tmoranlopez@mncn.csic.es

T. Moran-Lopez

Department of Biogeography and Global Change, National

Natural Science Museum (MNCN-CSIC), Serrano 115dpo.,

28006 Madrid, Spain

R. Poyatos � S. Sabate

CREAF, Cerdanyola del Valles, 08193 Barcelona, Spain

P. Llorens

Institute of Environmental Assessment and Water Research

(IDAEA-CSIC), Barcelona, Spain

123

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DOI 10.1007/s10342-013-0768-0

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Mediterranean montane forests are of particular interest

since changes in their composition can be used as early

global change sensors (Weber et al. 2007). The coexistence

of Eurosiberian populations at their southern distribution

limits and more xeric-adapted species makes these eco-

systems particularly sensitive to land use and/or climate

changes (Gimmi et al. 2010). For instance, a significant

shift from boreal Scots pines (Pinus sylvestris L.) to sub-

Mediterranean pubescent oaks (Quercus pubescens Willd.)

in dry valleys of the Alps has already been observed

(Gimmi et al. 2010; Rigling et al. 2013). In the Iberian

Peninsula, enhanced climatic constraints on radial growth

(Andreu et al. 2007; Martinez-Vilalta et al. 2008), and

drought-driven defoliation and mortality (Galiano et al.

2010; Heres et al. 2012) are all evident signs of Scots

pine’s intrinsic vulnerability to water deficits. Increased

competition due to the abandonment of management

practices may also aggravate the effects of drought on

demographic rates (Martinez-Vilalta et al. 2012; Vila-

Cabrera et al. 2011). Poor Scots pine regeneration in

declining populations together with an increased recruit-

ment of Quercus species (Galiano et al. 2010) points at a

potential substitution of Scots pine by more drought-tol-

erant species in dry, unmanaged sites (Vila-Cabrera et al.

2012).

Scots pine and pubescent oak show contrasting physio-

logical and growth responses to drought, which may

underlie directional vegetation shifts with increased aridity.

Under atmospheric and edaphic drought, Scots pine dis-

plays a strict stomatal control, while pubescent oak main-

tains moderate transpiration rates (Poyatos et al. 2008;

Zweifel et al. 2007) thanks to its tolerance of lower xylem

water potentials without suffering substantial cavitation

and its ability to extract water from deeper soil layers

(Valentini et al. 1992; Zweifel et al. 2007). Moreover,

Scots pine’s late bud-burst and growth initiation makes it

especially vulnerable to changes in summer water avail-

ability, as opposed to pubescent oak, which takes advan-

tage of higher water availability in spring by earlier radial

growth and leaf expansion (Zweifel et al. 2006). Accord-

ingly, Scots pine radial growth shows comparatively

stronger correlations with climatic variables associated

with summer water availability (Weber et al. 2007; Eil-

mann et al. 2011). In addition to species-specific variation,

climatic controls on radial growth can vary due to local

factors (e.g. Weber et al. 2007; Vachiano et al. 2012) and

also within a population (e.g. Heres et al. 2012). Moreover,

tree-level characteristics such as size, previous growth rate

or age mediate the effects of extreme drought events on P.

sylvestris growth (Martinez-Vilalta et al. 2012; Zang et al.

2012). In comparison, intrapopulation variability in Q pu-

bescens climate–growth responses has been comparatively

less studied.

Despite the existing wealth of dendroecological and sap

flow studies, the link between climate–growth relationships

and physiological regulation of tree water use has remained

relatively unexplored. In this regard, high water use effi-

ciency (WUE) for growth, estimated as the annual girth

increment per volume of water transpired (Breda and

Granier 1996), would probably confer a competitive

advantage in water-limited forests. Indeed, intrinsic WUE

measured in tree rings has shown considerable intrapopu-

lation variability, associated with drought-induced decline

processes in P. sylvestris (Voltas et al. 2013; Heres et al.

2013) and deciduous oaks such as Quercus robur (Levanic

et al. 2011).

Here, we analyse mid-term water use strategies and

long-term growth–climate relationships in Q. pubescens

and P. sylvestris stands in the pre-Pyrenees (NE Iberian

Peninsula), focusing on differences between species and

intrapopulation variability. Using a combination of den-

droecological and sap flow techniques, we (1) assessed

radial growth patterns of both species and their possible

relationships with climatic trends and (2) analysed intra-

population variability in drought sensitivity and its asso-

ciation with water use strategies and recent growth trends.

We hypothesised that P. sylvestris growth would be more

sensitive to reduce water availability, especially during the

recent decades, compared to Q. pubescens (H1). We also

postulated that both species would display intrapopulation

variation in drought responses (H2a), whereby drought-

sensitive trees would display higher initial growth rates and

a more strict stomatal control (H2b). As a result of

enhanced drought constraints in P. sylvestris, (H3) intra-

population variability in water use efficiency for growth

(WUEBAI) would be more tightly linked to growth sensi-

tivity to drought in P. sylvestris than in Q. pubescens.

Materials and methods

Study area

The experimental plots are part of the Vallcebre research

area (42�120N, 1�490E), located in the Eastern Pyrenees (NE

Iberian Peninsula). Climate is sub-Mediterranean, with an

average air temperature of 9 �C (measured at 1,260 m.a.s.l.)

and a mean annual precipitation of 826 ± 206 mm and an

annual potential evapotranspiration of about 823 mm (La-

tron et al. 2008). During the central part of the growing

season (April–August), potential evapotranspiration

(515.86 ± 4.14 mm, 1950–2010 mean ± SE) exceeds pre-

cipitation (470 ± 17.3 mm). Mudstone and sandstone are

the principal underlying lithologies in this area.

Three plots, all located within ca. 1.5 km from the vil-

lage of Vallcebre, were chosen for this study: two Scots

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pine stands and one oak stand. The lower Scots pine stand

(Cal Sort plot) is located in an abandoned terraced slope, at

an elevation of 1,260 m.a.s.l. Soil depth is ca. 65 cm and

has a sandy-loam texture (Rubio 2005). Stand density is

2,165 stems ha-1, and leaf area index (LAI) is 2.4 m2 m-2

(Poyatos et al. 2008). Tree mean diameter at breast height

(dbh) is 15.0 ± 0.7 cm, and the estimated average age of

dominant and co-dominant trees is 64 ± 6 years (n = 20).

The upper Scots pine stand (Cal Parisa plot) is located in a

southeast-facing slope (10–30 % of hillslope gradient) at

1,400 m.a.s.l. Within this plot, the soil has a silty-loam

texture. Stand density is 2,400 stems ha-1, and LAI is ca.

2.0 m2 m-2 (Llorens et al. 1997). Mean dbh is 17.3 cm,

and age of dominant and co-dominant trees is 63 ± 5 years

(n = 15). The oak stand (Cal Barrol plot) is located at

1,100 m.a.s.l., on a substrate formed by a loamy matrix and

limestone blocks (Rubio 2005). Tree density is 828 trees

ha-1, and whole-stand LAI is 3.35 ± 0.5 m2 m-2 (Muzylo

et al. 2012). Tree mean dbh is 21.1 ± 1.4 cm. Based on

tree ring analyses of wood cores extracted at breast height

(n = 14), the age of Q. pubescens trees was estimated to be

at least ca. 80 years old. At the plot level, a surrogate for

intra-specific competition for belowground resources was

calculated as the number of neighbours within a buffer

distance of 2.5 and 5 m from individual trees. This index

was significantly correlated with distances to the nearest

neighbours in both pine and oak stands (Pearson test

-0.54, P \ 0.05 and -0.68, P \ 0.01, respectively). Hence,

distance to nearest neighbour was used to assess focal trees

competence status for water sources in further analyses.

Meteorological data

Meteorological monitoring of Vallcebre research catch-

ments started in 1989 (Llorens and Gallart 1992). In situ

measured rainfall (P, mm), air temperatures (T, �C) and

potential evapotranspiration (PET, mm) series (1989–2010)

were used in this study. Potential evapotranspiration, based

on the Penman–Monteith FAO method, was calculated as

described in Llorens et al. 2010.

In order to extend the climatic time series back in time

(period 1956–1988), Vallcebre climatic data were esti-

mated from nearby meteorological stations belonging to

the Spanish Meteorological Agency (AEMET) at Berga

(12 km from the study site) and La Molina (20 km from

the study site). We fitted generalised mixed models, and a

good agreement was found for both air temperatures

(R2 = 0.97) and precipitation (R2 = 0.84). During this

period (1956–1988), PET was estimated using the Thorn-

thwaite method and rescaled using a fitted relationship

obtained between Thornthwaite PET and Penman–Mon-

teith PET (R2 = 0.92). Two indexes of climatic drought

stress were calculated: (1) the ratio between annual

precipitation and potential evapotranspiration (P/PET;

UNEP 1992), which was used to analyse the drought

responses of tree growth and (2) a drought index (Di),

estimated as the difference between accumulated precipi-

tation and potential evapotranspiration from April to

August (Rigling et al. 2013). The value of Di was used to

compare the drought conditions in our study site with other

locations.

Tree ring chronology building and BAI calculation

In April 2010, 15 and 14 dominant or co-dominant trees

were sampled from the lower and the upper Scots pine

stands, respectively; 14 trees were sampled in the oak plot.

Mean dbh was 21.4 ± 2.0 cm for P. sylvestris and

23.9 ± 2.2 for Q. pubescens. Two cores were extracted to

the pith at breast height from each tree. All samples were

visually cross-dated and measured using Windendro soft-

ware (Regent Instrument Inc. 2002). The resulting series

underwent a cross-dating quality control with the statistical

programme COFECHA (Holmes, 1983). Subsequently,

series of the same stem were averaged, and annual basal

area increment estimated (BAI, mm2/year). A preliminary

analysis of growth trends in both Scots pine plots showed

that there were no significant differences between them

(P [ 0.05); therefore, all Scots pines were pooled together

for further analyses.

Sap flow, canopy stomatal conductance and water use

efficiency for growth

In the lower Scots pine plot and the oak plot, sap flow,

meteorological variables and soil moisture (0–30 cm) were

measured continuously and simultaneously from June 2003

to September 2005. A maximum of 14 P. sylvestris and 12

Q. pubescens were equipped with sap flow sensors. Tech-

nical details on the experimental setup of both plots can be

found in Poyatos et al. (2005). Sap flow density in the outer

xylem was measured using heat dissipation probes

according to Granier (1985). The procedure to upscale sap

flow in the outer xylem to the whole tree level was the

same for all trees and involved the correction for radial

variability in sap flow density and the estimation of sap-

wood depth using site-specific allometric relationships

(Poyatos et al. 2007; 2008). Tree leaf areas were also

obtained using local allometric relationships obtained from

forest inventory data (Gracia et al. 2000–2004; http://www.

creaf.uab.es/iefc/).

Time series of daily tree sap flow contained some

missing data (5.43 % on average). Since we were inter-

ested in total transpiration during the central part of the

growing season (June, July and August), days with missing

data were gap-filled using either fitted relationships

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between sap flow of neighbouring trees (R2 = 0.68 on

average) or values for days with similar environmental

conditions.

Midday canopy stomatal conductance (Gs,md) was cal-

culated with the simplified Penman–Monteith equation for

aerodynamically rough canopies (Whitehead and Jarvis

1981):

Gs;md ¼ckJL;md

qcpDmd

ð1Þ

where c is the psychrometric constant (kPa K-1), k is latent

heat of vaporisation of water (J kg-1), q is air density

(kg m-3), cp is specific heat of air at constant pressure

(J kg-1 K-1), and D (kPa) is vapour pressure deficit, and

JL,md is leaf-area-based sap flow averaged for the midday

hours (11:00 to 14:00) and converted to molar units

(mmol m-2 s-1).

Water use efficiency for growth (Breda and Granier

1996) was calculated here as the individual basal area

increment divided by the volume of water transpired from

early June to the end of August (WUEBAI). As current-year

growth could depend on physiological processes occurring

during the previous year, WUEBAI was calculated based on

both current and previous-year transpiration.

Data analysis

All data analyses, unless otherwise stated, were carried out

using the R statistical software (2011). Linear mixed

models were fitted using nlme package (Pinheiro et al.

2012), selecting the model with the lowest Akaike infor-

mation criterion (AIC). In order to evaluate climate–growth

relationships, Pearson correlations between BAI and aver-

age air temperatures and total rainfall were estimated on a

monthly basis and for all individual trees. Preliminary

examination of mean annual temperatures showed consid-

erably more years with positive anomalies over the last

two, and BAI curves revealed more erratic and acute peaks

(decades compared to previous years 1956–1989) (Fig. 1).

Hence, water availability effects on tree growth in both

time periods (1956/1960–1990 and 1991–2010) were

assessed using linear mixed models. Our response variable

was ln(BAI ? 1), and predictor variables were summer

P/PET, time period and the interaction between both. Tree

identity was included as a random variable, and year was

introduced with a first-order autoregressive structure in

order to account for temporal autocorrelation. Subse-

quently, summer P/PET effects on growth were analysed

separately for both periods.

In order to evaluate intrapopulation variability in

drought sensitivity, individual climate–growth correlation

coefficients were introduced into a principal components

analysis. In this analysis, only climatic variables which had

shown the highest signals on tree growth during the entire

period (1960–1990) were considered. The first component

of the PCA (PC1) explained 61 and 58 % of the variance

for P. sylvestris and Q. pubescens, respectively. PC1 was

thus interpreted as a measure of drought tolerance since it

was highly related to individual trees’ responses to summer

temperature and precipitation. In both species, trees which

loadings in the first component were clearly related to

Fig. 1 a Annual rainfall (mm) and b mean annual temperature (�C)

from 1956 to 2010. Continuous line indicates linear regression of

temporal trends. c Basal area increment (mm2/year, mean ± standard

error) of Q. pubescens (open circles) and P. sylvestris (black circles)

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positive temperature effects on growth and lower summer

precipitation responses were considered ‘drought tolerant’,

those which displayed the opposite pattern were considered

‘drought sensitive’ and those with loadings close to zero

were considered as ‘intermediate’ (cf. ‘Results’ section).

Additionally, a k-means analysis was performed so as to

ensure climate–growth groups coherence. PCA and k-

means analysis were carried out with Primer 6 (Primer-e

Ltd, Lutton, UK) and Gingko software (De Caceres et al.

2007), respectively.

Linear models were used to disentangle the relative

effect of water use strategies and initial growth rates

(ln(BAI60–90 ? 1) from 1960 to 1990) on individual trees

drought tolerance. Our response variable was individual

trees’ projection on the first axis of the PCA in the direction

of positive temperature effects (PC1 for oaks and -PC1 for

pines), and the explanatory variables were individual pines

WUEBAI, ln(BAI60–90 ? 1) and their interaction. Besides,

changes in competitive status of trees according to drought

tolerance and time period were tested through linear mixed

models. Our response variable (BAIrel) was calculated as:

BAIrel ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi

BAIi�

BAI

q

ð2Þ

where BAIi is individual tree BAI and BAI is average stand

BAI. Predictor variables were drought-tolerance group

membership, time period and both variables interaction.

Tree identity was introduced as random effect.

In order to relate drought sensitivity of growth with tree-

specific stomatal control of gas exchange, we summarised

the variation in Gs,md with respect to vapour pressure

deficit and soil water content, using two well-known

mathematical formulations with strong physiological

foundations. The sensitivity of Gs,md to vapour pressure

deficit (D, kPa) was analysed using the following rela-

tionship (Oren et al. 1999):

Gs;md ¼ Gs;ref � m ln D ð3Þ

This equation was fitted using the quantile regression

technique as implemented in the R package quantreg

(Koenker Team 2008). We chose s = 0.95 (i.e. 95th

quantile), and we assumed that it was representative of the

relationship between Gs,md and ln D when other factors

were optimal (Cade and Noon 2003). The obtained

intercept and slope equalled Gs,ref (reference Gs at

D = 1 kPa) and m (sensitivity to vapour pressure deficit,

-dGs,md/d ln D), respectively (Oren et al. 1999). Only data

with average midday D [ 0.6 kPa were analysed, to avoid

potential errors in Gs estimation under low evaporative

demand (Ewers and Oren 2000).

Canopy conductance usually shows a threshold-like

response to soil water availability (e.g. Granier et al. 2000).

The response of Gs,md to soil water content was thus

analysed using a linear segmented regression, which

identifies the break point in soil water content below which

Gs,md starts to decline in a linear fashion (Muggeo 2008).

Preliminary analyses for Q. pubescens showed very little

sensitivity of Gs,md to soil moisture within 0–30 cm, in line

with previous results (Poyatos et al. 2008); hence, we only

carried out the analyses for Scots pine. The soil water

content threshold for transpiration decline was thus con-

sidered as an indicator of tree-level sensitivity to water

availability in the soil.

Results

Climate trends

Annual rainfall in the study site (Fig. 1a) significantly

decreased during the period 1956–2010 (R2 = 0.18,

P \ 0.05) with an average reduction of 5.75 mm/year. For

the same period, mean annual temperature (Fig. 1b) sig-

nificantly increased (R2 = 0.32, P \ 0.05), at an average

rate of 0.02 �C/year. Besides, the analysis of mean annual

temperatures revealed two different periods over the last

decades with respect to the frequency of positive temper-

ature anomalies. Between 1956 and 1990, 14.3 % of the

years showed positive temperature anomalies while it

amounted to 40 % over the 1991–2010 period. Such dif-

ferences between periods were not found for the frequency

of negative anomalies of annual rainfall (23.5 and 33.3 %

of years with negative anomalies, respectively). Regarding

summer drought, in the 1956–1989 period, the value of Di

(mean ± SE) was 4.11 mm ± 21.83, while during

1991–2010 Di dropped to -126 ± 31.06 mm and

remained below -300 mm for 14.2 % of the years.

Growth patterns and climate–growth relationships

Growth trends differed between species at the beginning of

the study period, but, from the 1970s onwards, P. sylvestris

and Q. pubescens showed similar growth trends. The time

series of BAI did not reveal an acute average loss of growth

potential for any species, but, over the last decades, an

enhanced jagged pattern in BAI was observed (Fig. 1c).

Pinus sylvestris BAI was correlated with both previous-

year and current-year climatic conditions (Fig. 2a, c).

During the 1960–1990 period, annual growth was mainly

positively correlated with winter temperatures (Fig. 2a). In

contrast, negative correlations between BAI and tempera-

ture were typically observed during the 1991–2010 period,

especially for current summer months. Moreover, the weak

relationships between BAI and rainfall observed during

1960–1990 turned to high, positive correlations during the

1991–2010 period (Fig. 2c). Accordingly, summer P/PET

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only showed positive, significant effects on P. sylvestris

growth over the last twenty years. Besides, a change in

growth sensitivity to summer P/PET over the last decades

was detected (Table 1).

Likewise, Q. pubescens climate–growth relationships

embraced both previous-year and current-year conditions

(Fig. 2). During the 1960–1990 period, positive correla-

tions between BAI and monthly temperature were gener-

ally observed; particularly, warmer springs were

accompanied by enhanced growth. In comparison, during

the 1991–2010 period, more negative correlations were

found (Fig. 2b). In contrast, an increased frequency of

positive correlations between BAI and precipitation was

observed during the 1991–2010 period, especially during

winter and summer months (Fig. 2d). When analysing the

complete Q. pubescens BAI time series, enhanced growth

sensitivity to summer P/PET was observed as well as a

positive and highly significant effect of P/PET on BAI

when the 1991–2010 period was analysed separately

(Table 1).

Intrapopulation variability in climate–growth

relationships, WUEBAI and recent BAI trends

We observed intrapopulation differences in climate-

growth relationships of both species, associated with a

gradient of drought sensitivity (Fig. 3; cf. ‘Meterials and

methods’ section). Trees were grouped as ‘drought sensi-

tive’ (9 pines and 5 oaks), ‘drought tolerant’ (5 pines and 3

oaks) and ‘intermediate’ (14 pines and 6 oaks). PCA

groups were also coherent with k-means analysis (92.86 %

of coherence, TESS = 5.69, pseudo-F = 27.10). These

groups also showed different temporal growth trends

(Fig. 4a, b) but did not significantly differ in their distances

Fig. 2 Pearson correlation coefficient between basal area increment

(mm2/year) and a, b mean monthly temperatures (�C) or c, d monthly

rainfall (mm). Left panels correspond to P. sylvestris and right ones to

Q. pubescens. Black columns correspond to 1960–1990 period and

grey ones to 1991–2010. More than 50 % of trees with significant

correlations (P \ 0.05) are indicated by solid triangles and more than

30 % by solid dots. Previous year months are shown in capitals and

current months in lowercase

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to the nearest neighbour (P = 0.58 and P = 0.87, in oaks

and pines, respectively).

‘Drought-sensitive’ P. sylvestris, which displayed higher

initial growth rates but current growth decline (Fig. 4a),

also showed significantly lower WUEBAI (Fig. 4c;

mean ± SE = 0.23 ± 0.01 mm2/l H2O, P \ 0.01). The

opposite pattern (no symptoms of growth decline as well as

high WUEBAI) was found in drought-tolerant trees (Fig. 4a,

c; mean ± SE = 1.01 ± 0.12 mm2/l H2O). In accordance,

WUEBAI and initial growth rates had positive and negative

effects, respectively, on P. sylvestris growth sensitivity to

drought (see Table 3), albeit only marginally for initial

growth. In addition, there was a significant shift of ten-

dency in the competitive status of trees, as measured by

their BAIrel, which varied across climate–growth groups

and the time period considered (Table 2; Fig. 4a).

In contrast, Q. pubescens growth trends and WUEBAI

did not show large differences among groups (Fig. 4, right

panels). Besides, neither water use strategies nor initial

growth rates had significant effects on drought tolerance

(Table 3). Nonetheless, some among-groups differences

were observed in growth trends, but only during the 1970s

and 1980s, when drought-sensitive trees showed a stronger

growth response (Table 2; Fig. 4b) to particularly mild

climatic conditions during that period (Fig. 1a). These

differences vanished during the 1990s, and recent growth

now shows a slight decline for all groups (Fig. 4b).

Differences in biomass allocation and size

between climate–growth groups

P. sylvestris growth was significantly related to basal area

(P\ 0.01), and all groups showed similar size–growth patterns

(Fig. S1). Similarly, accumulated transpiration was positively

related to tree leaf area, with analogous responses between

groups. Some but not all ‘drought-sensitive’ pines tended to

show remarkably higher leaf areas (Fig. 4e) although no dif-

ferences in leaf area were found between ‘drought-sensitive’

and ‘drought-tolerant’ pines (P = 0.10). However, we did

observe a significantly lower leaf to sapwood area ratio (AL:AS)

in ‘drought-sensitive’ pines (0.059 ± 0.002 m2 cm-2) com-

pared to ‘drought-tolerant’ pines (0.071 ± 0.003 m2 cm-2,

P \0.01). For Q. pubescens, BAI was highly related to tree

basal area (Fig. S1) and tree transpiration to leaf areas (Fig. 4f),

without any obvious difference among climatic growth sensi-

tivity groups. Nonetheless, ‘drought-sensitive’ oaks showed

the highest basal areas, and ‘drought-tolerant’ oaks showed the

smallest leaf areas (Figs. 4f and S1).

Tree-specific stomatal control related to growth

sensitivity to climate

With regard to P. sylvestris stomatal control, parameter

m of the stomatal response to D followed a common

relationship with respect to Gs,ref, meaning that stomatal

Table 1 Results of the linear mixed models of P. sylvestris and Q. pubescens BAI response to summer water availability, applied to different

time periods

Species Time period of

the analysis

Predictor variables Estimate SE t value P AIC

P. sylvestris 1960–2010 Intercept 6.11 0.08 73.78 <0.001 1467.86

P/PET 0.05 0.04 1.22 0.22

(1991–2010) 0.02 0.08 0.19 0.85

P/PET 3 1991–2010 0.32 0.06 5.68 <0.001

1960–1990 Intercept 6.16 0.09 65.30 <0.001 848.28

P/PET 0.05 0.04 1.21 0.23

1991–2010 Intercept 6.14 0.10 63.67 <0.001 631.31

P/PET 0.37 0.04 8.50 <0.001

Q. pubescens 1960–2010 Intercept 5.80 0.14 40.29 <0.001 429.61

P/PET 0.05 0.04 1.23 0.22

(1991–2010) -0.02 0.10 -0.17 0.87

P/PET 3 1991–2010 0.22 0.06 3.46 <0.001

1960–1990 Intercept 5.88 0.14 41.39 <0.001 319.25

P/PET 0.05 0.05 1.10 0.27

1991–2010 Intercept 5.78 0.17 33.54 <0.001 103.79

P/PET 0.28 0.04 6.50 <0.001

For the analysis covering the period 1960–2010, the response variable was ln(BAI ? 1) and predictor variables were P/PET (mean summer rainfall/

potential evapotranspiration) and time period (1960–1990 or 1991–2010). The period 1960–1990 was used as the reference level. Additional

analyses were also performed where ln(BAI ? 1) was modelled as a function of P/PET for the two separate periods (1960–1990 vs. 1991–2010).

Significant effects (P \ 0.05) are shown in bold. AIC is Akaike information criterion, and SE represents the standard error of the estimate

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sensitivity to D was similarly predicted by gas exchange

capacity for all trees, and no grouping was observed

(Fig. 5c). However, trees within the ‘drought- sensitive’

group showed significantly higher Gs,ref values (mean ±

SE = 248 ± 15 mmols m-2 s-1) than the ones obtained

for the rest of the pines (mean ± SE = 138 ± 18 mmols

m-2 s-1; t test, P = 0.001; Fig. 5a). The soil water content

threshold below which Gs started to decline was also

marginally higher (P = 0.06) for the ‘drought-sensitive’

pines (mean ± SE; 0.26 ± 0.02 cm3 cm-3) compared to a

value of 0.21 ± 0.02 cm3 cm-3 observed for the rest of the

pines. Hence, pines which displayed a radial growth more

sensitive to drought closed stomata at comparatively higher

soil water availability. For Q. pubescens, we also observed

that m and Gs,ref of individual trees followed a common

relationship (slope = 0.86, R2 = 0.96; Fig. 5d). However, in

this case, ‘drought-sensitive’ trees displayed lower Gs,ref

values (mean ± SE = 73 ± 22 mmols m-2 s-1) than the

ones obtained for the rest of the oaks (mean ± SE =

129 ± 17 mmols m-2 s-1; t test, P = 0.022; Fig. 5b).

Discussion

Recent shifts in climate–growth relationships

towards enhanced drought constraints

Globally, climatic conditions reported in the Vallcebre

research area are milder than those found in other Med-

iterranean forests in which symptoms of Scots pines

decline in terms of decreased annual growth, increased

mortality rates and reduced regeneration potential have

been observed. For instance, annual precipitation is on

average 200 mm higher than in Valais (Swiss Rhone

valley; Weber et al. 2007; Rigling et al. 2013), Italian

Aosta valley (Vertui and Tagliaferro 1998; Vachiano

et al. 2012) and central Pyrenees (Galiano et al. 2010;

Heres et al. 2012). However, summer drought can be

severe. On average, summer potential evapotranspiration

(PET) is higher than in Valais, and water shortage

(measured in terms of P-PET) can occasionally reach

values similar to those associated with increased Scots

pines mortality (below -300 mm; Rigling et al. 2013).

Hence, even though the Vallcebre basin can be considered

a relatively mesic site for both species, tree transpiration

can be strongly reduced during summer drought, espe-

cially in Scots pine (Poyatos et al. 2008; Llorens et al.

2010).

Recent trends in air temperature and rainfall show

increasing drought constraints in the studied stands con-

sistent with results observed in other montane forests

within the Pyrenees (Heres et al. 2012). Differences among

species in growth trends at the beginning of the study

period (1950–1960) may be reflecting differences in the

maturity of stands (pines were sapling, while oaks were

mature trees). However, tree ring data after BAI stabilisa-

tion (1960 onwards) allowed us to avoid initial stand

development growth signals in further analyses (LeBlanc

Fig. 3 Principal components analysis (PCA) with growth–climate

correlation indexes from 1960 to 2010 for a P. sylvestris and b Q.

pubescens. Points correspond to the projection of individual trees

growth responses. Original variables in the PCA (P = monthly total

precipitation, T = monthly average temperature) are marked by

arrows; previous year months are shown in capitals and current

months in lowercase. The black circle corresponds to the correlation

coefficient = 1 between principal components and sample variables

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1990). Since the 1970s, P. sylvestris and Q. pubescens have

displayed, on average, similar growth patterns. In accor-

dance with climatic trends (Fig. 1a, b), climate–growth

relationships showed a change in tendency towards

enhanced summer drought constraints in recent years for

both species (Fig. 2; Table 1).

Fig. 4 Basal area increment (BAI; mm2/year) in P. sylvestris a and

Q. pubescens b trees in the three different climate–growth groups.

Error bars depict SEs of the mean. Relationship between accumu-

lated transpiration during the months of June to August (l H2O/tree)

and annual growth (BAI) for P. sylvestris (c) and Q. pubescens (d).

The slope of the linear regression (continuous line) between both

variables is water use efficiency expressed in terms of BAI (WUEBAI,

annual accumulated per annual growth). Relationship between leaf

area (m2) and June–August transpiration for P. sylvestris (e) and Q.

pubescens (f). In c–f, each point is an individual tree over 1 year and

represents the accumulated transpiration from June to August

(2003–2005). Note that the scale of the y axis in c and d is different

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Pinus sylvestris growth was mainly related to winter

temperatures over the 1960–1990 period while linked to

milder summer droughts over the last two decades (Fig. 2a,

c; Table 1). This change in tendency is in accordance with

previous studies showing enhanced climatic constraints on

P. sylvestris growth over the last decades among different

Iberian populations (Martinez-Vilalta et al. 2008) and

consistent with our hypothesis H1. We also observed a shift

in climate–growth relationships for Q. pubescens, from

winter–spring temperatures constraints to summer water

availability limitations (Fig. 2b, d; Table 1). Such shifts

towards increased growth sensitivity to water availability

were quite unexpected here, given the comparatively lower

drought constraints on growth displayed by Q. pubescens

elsewhere (Weber et al. 2007).

Additionally, recent changes in forest structure may have

enhanced competition for belowground resources, espe-

cially water, in these Mediterranean mountain forests. The

studied P. sylvestris stands are located in old agricultural

terraces abandoned in the early 1950s and thus subjected to

forest densification processes (Poyatos et al. 2003). Stand

density in these areas (cf. ‘Materials and methods’ section)

is much higher than the average density of Scots pine stands

in Catalonia (629.18 trees ha-1; IEFC, Gracia et al. 2000–

2004; http://www.creaf.uab.es/iefc/). High stand basal areas

and densities reduce growth potential in P. sylvestris and

may aggravate climatic constraints (Vila-Cabrera et al.

2011; see Martinez-Vilalta et al. 2012 and references

therein). In fact, stand density has been pointed out as a

predisposing factor for drought-induced crown damage and

mortality in unmanaged Scots pines stands or plantations

(Galiano et al. 2010; Sanchez-Salguero et al. 2012). Similar

processes after the abandonment of management may have

occurred in the Q. pubescens stand, as it presently shows a

dense understory and a relatively high stand LAI (Muzylo

et al. 2012). Hence, the enhanced vulnerability to summer

drought observed for both species in this study is probably

the result of the combined effect of increased climatic

aridity and enhanced competition for water. Thinning

would reduce competition intensity and enhance growth,

but increasing drought conditions would probably continue

to constrain the maximum sustainable basal area, as

recently reported for a xeric P. sylvestris stand (Giuggiola

et al. 2013).

Table 2 Results of the linear mixed models relating tree relative BAI (BAIrel), as a measure of competitive status of individual trees, to climate–

growth group (drought tolerant, drought sensitive or intermediate) and time period (1960–1990 and 1991–2010), for P. sylvestris and Q.

pubescens

Species Predictor variables df F value P AIC

P. sylvestris Intercept 1373 734.15 <0.001 112.08

Group 26 0.65 0.531

Period 1373 16.57 <0.001

Group 3 period 1373 73.68 <0.001

Q. pubescens Intercept 663 205.08 <0.001 -137.54

Group 12 0.61 0.560

Period 663 10.87 <0.001

Group 3 period 663 30.62 <0.001

Significant effects (P \ 0.05) are shown in bold. AIC is Akaike information criterion, and SE represents the standard error of the estimate

Table 3 Results of the linear model of climate–growth characteristics as a function of water use efficiency for growth (WUEBAI) and ln-

transformed initial growth rates (ln(BAI60–90 ? 1))

Species Predictor variables Estimate SE t value P AIC

P. sylvestris Intercept 12.36 8.048 1.536 0.15 71.21

WUEBAI 6.423 1.742 3.688 <0.005

ln(BAI60–90 1 1) -2.562 1.206 -2.125 0.05

Q. pubescens (Intercept) -0.110 0.743 -0.269 0.793 64.50

WUEBAI 0.007 0.004 1.481 0.167

The response variable is the individual tree loading on the first principal component (PC1), resulting from the PCA of climate–growth

relationships (Fig. 3). We used values of -PC1 for P. sylvestris and PC1 for Q. pubescens, so that higher, positive values represent increasing

growth sensitivity to drought. Significant effects (P \ 0.05) are shown in bold. AIC is Akaike information criterion and SE represents the

standard error of the estimate

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Intrapopulation variability in climate–growth

relationships

For both species, we observed intrapopulation clustering

of climate–growth relationships, supporting our hypothe-

sis H2a. Our results showed that ‘drought-sensitive’ P.

sylvestris, which displayed the highest initial growth rates,

have suffered a loss of growth potential over the last

decades (Fig. 4a). In contrast, ‘drought-tolerant’ pines,

which showed a more conservative initial growth,

increased their growth rates after the 1980s and currently

maintain the highest BAI (Fig. 4a). These results point to

a significant shift in the competitive status of individual

trees associated with drought sensitivity (Table 2). The

opposite pattern has been found in a recent study on the

effects of extreme drought events on P. sylvestris growth.

Fast-growing trees resulted more affected by drought in

terms of immediate and delayed growth but continued

having the highest basal area increments after drought.

Hence, intrapopulation competitive relationships were not

affected (Martinez-Vilalta et al. 2012). However, that

study focused on the effects of a single extreme drought

event in the 1980s while here we consider overall growth

trends over the last two decades. The present growth

decline of initially fast-growing trees (Fig. 4a) may be

reflecting a response to gradually increasing dryness

(Fig. 1a, b) rather than the effects of a single and acute

drought episode.

With regard to Q. pubescens, the PCA also splits up

oaks in three different groups with different drought tol-

erances (Fig. 3b). Although all climate–growth archetypes

are currently showing similar growth patterns, ‘drought-

sensitive’ oaks were favoured under enhanced water

availability during the 1970s–1980s, while under recent

drier conditions, all climate–growth groups showed incip-

ient symptoms of growth decline (Fig. 4b). Unlike for P.

sylvestris, climatic constraints are not as important drivers

of shifts in intraspecific competitive relationships of Q.

pubescens at the studied site since all groups currently

show similar growth trends.

Fig. 5 a Reference canopy stomatal conductance (Gs,ref) of drought-

sensitive pines (n = 3) with respect to the rest of the pines (drought

tolerant and intermediate, n = 10), b Gs,ref of drought-sensitive

pubescent oaks (n = 5) and the rest of the oaks (n = 7). Relationship

between Gs,ref and sensitivity to vapour pressure deficit (m) of P.

sylvestris (c) and Q. pubescens (d). **P \ 0.01, *P \ 0.05

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Intrapopulation variability in climate–growth

relationships associated to water use regulation

Interestingly, for both species, this intrapopulation vari-

ability in climate–growth relationships seemed to be linked

to different water use strategies. ‘Drought-sensitive’ pines

(Fig. 3a) showed higher gas exchange potential (i.e. higher

Gs,ref) and lower WUEBAI compared to ‘drought-tolerant’

pines, which displayed lower Gs,ref and higher WUEBAI

(Figs. 4c,5a). No differences were found in the relationship

between m and Gs,ref among pines (Fig. 5c) suggesting that

‘drought-sensitive’ P. sylvestris did not differ in their rel-

ative stomatal regulation with respect to D (Poyatos et al.

2007). However, in absolute terms, they were indeed more

sensitive to D due to their higher values of m and Gs,ref.

‘Drought-sensitive’ trees also closed stomata at higher soil

water content values. As we only measured average plot

soil water content (i.e. not associated to individual trees),

this behaviour could result from either within-site spatial

variability in soil water availability for trees or differences

in rooting patterns between ‘drought-sensitive’ and

‘drought-tolerant’ pines. Enhanced physiological sensitiv-

ity to drought was related to reduced biomass allocation to

transpiring vs. conducting tissue, as ‘drought-sensitive’

pines showed consistently lower AL:AS compared to

‘drought-tolerant’ pines. These results are consistent with

patterns across climatic gradients (Poyatos et al. 2007) and

within-population differences between declining and non-

declining P. sylvestris (Poyatos et al. 2013).

The opposite pattern was observed for Q. pubescens,

whereby ‘drought-sensitive’ individuals showed reduced

Gs,ref and m values (Fig. 5b, d). In addition, sap flow is

relatively insensitive to superficial soil moisture in Q. pu-

bescens (Poyatos et al. 2008), so we could not explore

differences in soil water content thresholds for stomatal

closure. Both results agree with the ability of this species to

tap deep water sources (Valentini et al. 1992) and suggest

that ‘drought-sensitive’ trees may display comparatively

less developed root systems, thus explaining structural

constraints on gas exchange potential (i.e. reduced Gs,ref)

(Sperry et al. 1998). Overall, these findings show that

stomatal regulation of transpiration and climatic controls

on radial growth is tightly linked (hypothesis H2b), but in

different ways for P. sylvestris and Q. pubescens.

Other factors such as size (Zang et al. 2012) or crown

class membership (Martin-Benito et al. 2008) could also

underlie the observed intrapopulation variability in cli-

mate–growth relationships (but see Merian and Lebour-

geois (2011) for a counterexample of little size-related

variation in climate–growth relationships in P. sylvestris

and Quercus petraea). Our sampling strategy would have

minimised these size and social position effects as all trees

were codominant, showed similar heights and a small range

of dbh values. Indeed, our results show that climate–growth

groups were not associated with competition for below-

ground resources.

Implications for drought-induced decline processes

Even though no apparent symptoms of Scots pine drought-

induced decline have been observed in the study area, the

possibility that ‘drought-sensitive’ trees may have entered

a decline process cannot be discarded, given the gradual

decrease observed in BAI for ‘drought-sensitive’ and

‘intermediate’ trees (Fig. 4a). A long, gradual growth

decline has been shown to precede tree death in drought-

exposed Scots pine populations and has also been linked to

an enhanced climatic sensitivity of radial growth (Bigler

et al. 2006; Heres et al. 2012), as we have reported here.

Our results on intrapopulation variability in drought sen-

sitivity are consistent with coupling between climate,

growth and WUE (Voltas et al. 2013) and/or a limited

increase in WUE with increasing atmospheric CO2 con-

centration in P. sylvestris (Heres et al. 2013) as symptoms

of incipient drought-induced decline. Given the high stand

density in the study area, coupled with the current trend of

increasing aridity (Fig. 1), the studied population may

become vulnerable to drought-induced dieback in the fol-

lowing decades, as it has already been observed in other

unmanaged Scots pine populations in the Pyrenees (Gali-

ano et al. 2011). Nevertheless, ‘drought-tolerant’ individ-

uals increased their growth rates after 2005, a dry year

(Poyatos et al. 2008) which triggered forest decline epi-

sodes elsewhere in the Pyrenees (Heres et al. 2012). This

recovery occurred in response to a recent transient increase

in annual rainfall (Fig. 1a) and demonstrates that resilient

individuals can recover after drought.

In comparison, the evidence in scientific literature for

drought-induced decline in Q. pubescens is scarce (but see

Carnicer et al. 2011, Supp. Information, pp. 12–13). Despite

that in our study site Q. pubescens leaf water potentials

(Poyatos et al. 2008) are far from those values known to

induce leaf desiccation and senescence (Damesin et al.

1998), its moderate stomatal control in response to high

evaporative demand (Zweifel et al. 2007; Poyatos et al.

2008) can cause shoot dieback under extremely dry spells

(Zweifel et al. 2006; Nardini et al. 2013). According to a

recent monitoring programme of forest decline recently

started in Catalonia (NE Spain), 4 % of the total area

occupied by Q. pubescens was affected by crown dieback in

2011, including populations in the Pyrenees (Banque et al.

2011; P. Llorens, personal observation). These results are

consistent with the increasing drought constraints on growth

observed for Q. pubescens since the 1990s (Fig. 4b).

Other deciduous oaks in Europe have indeed shown

vulnerability to drought-induced decline (e.g. Breda et al.

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2006). For one of these species, Quercus robur, BAI

trends, wood anatomical traits and gas exchange patterns

revealed that fast-growing trees showed lower WUE and

wider vessels, which resulted in increased predisposition to

drought-related mortality (Levanic et al. 2011). Likewise,

the combined monitoring of water use and growth strate-

gies in potentially vulnerable populations of Q. pubescens

would shed some light on the physiology behind climatic

controls on growth under severe drought, and how these

mechanisms vary within a population.

Conclusions

Our results reveal increasing growth constraints over the last

decades for P. sylvestris and for Q. pubescens. These patterns

may be the result of a concomitant increase in aridity and the

lack of forest management. However, drought responses of

growth and physiological traits were not uniform within

species. Drought sensitivity was closely related to tree-spe-

cific past growth trends and water use regulation in P. syl-

vestris. In contrast, within-population differences in drought

sensitivity and water use traits did not result in different

growth trends in recent decades among Q. pubescens indi-

viduals. Here, we also show that the initially slowest-grow-

ing P. sylvestris eventually became more resilient and

recovered faster after recent drought-induced declines in

growth, leading to a shift in intrapopulation competitive

relationships. Although increasing drought constraints may

be contributing to the substitution of P. sylvestris by Q. pu-

bescens in dry sites (Galiano et al. 2010; Rigling et al. 2013),

we observed an incipient growth decline in Q. pubescens,

which may be punctuated by the occurrence of extreme

drought episodes. Overall, this study sheds some light on the

key physiological and growth regulation mechanisms, which

may be involved in the onset of gradual tree decline. How-

ever, future studies including larger spatial scales and

incorporating aridity and stand density gradients may be

needed in order to make species-level generalisations.

Acknowledgments This study was supported by MONTES

(CSD2008-0040) funded by Spanish Government. TM-L was bene-

ficiary of a ‘Fundacion la Caixa’ grant, and RP was supported by a

Juan de la Cierva postdoctoral fellowship. We acknowledge help of

Garcıa-Estrıngana P. and Latron J. in field data acquisition, Riera J.L.

in data analysis Gutierrez E. in dendroecological study, Delgado J. for

providing us long-term climatic databases and Valladares F. for

carefully reading this manuscript.

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