Content uploaded by Lluís Coll
Author content
All content in this area was uploaded by Lluís Coll on Dec 05, 2015
Content may be subject to copyright.
Forest Systems
24(3), e042, 10 pages (2015)
eISSN: 2171-9845
http://dx.doi.org/10.5424/fs/2015243-07469
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)
RESEARCH ARTICLE OPEN ACCESS
extreme temperatures, or severe drought, yew is re-
stricted to favorable niches that are protected from
these extreme conditions (Thomas & Polwart, 2003).
Consequently, in the Mediterranean region, yew trees
usually grow in isolated populations in shady mountain
ravines and on cliffs, or as a sub-canopy tree in a
Forest structure of Mediterranean yew (Taxus baccata L.)
populations and neighbor effects on juvenile yew performance
in the NE Iberian Peninsula
Pere Casals1*; Jordi Camprodon1,2; Antònia Caritat1,3; Ana I. Ríos1; David Guixé1; Xavier Garcia-Martí4;
Santiago Martín-Alcón1; Lluis Coll1
1 Forest Sciences Centre of Catalonia (CTFC-CEMFOR), Crta. Sant Llorenç de Morunys, Solsona, Lleida, Spain
2 BETA Technological Center. Universitat de Vic-Universitat Central de Catalunya. Vic, Catalonia, Spain
3 Universitat de Girona. Girona, Catalonia, Spain. 4 Bioma Forestal, Etxauri, Navarra, Spain
Abstract
Aim of study: In the Mediterranean region, yew (Taxus baccata L.) usually grows with other tree species in mixed forests. Yew
recruitment and juvenile growth may depend on the structure of the forest and the net balance between competition for soil water
and nutrients with neighbors and facilitation that these neighbors exert by protecting the plants from direct sun exposure. This study
aims, at a regional scale, to analyze the structure of forests containing yew, and, on an individual level, to analyze the effect of the
surrounding vegetation structure on the performance of yew juveniles.
Area of study: The structural typologies of yew populations were defined based on field inventories conducted in 55 plots dis-
tributed in 14 localities in the North-Eastern (NE) Iberian Peninsula, covering a wide range of yew distribution in the area. In a
second step, an analysis of neighboring species’ effects on juveniles was conducted based on the data from 103 plots centered in
yew juveniles in five localities.
Main Results: A cluster analysis classified the inventoried stands into four forest structural types: two multi-stratified forests
with scattered yew and two yew groves. Multiple regression modeling showed that the δ13C measured in last year’s leaves posi-
tively relates to the basal area of conifer neighbors, but negatively with the cover of the yew crown by other trees.
Research highlights: At a stand-level, the density of recruits and juveniles (625 ± 104 recruits ha–1, 259 ± 55 juveniles ha–1) in
mixed forests was found to be higher than that on yew dominant stands (181 ± 88 recruits ha–1 and 57 ± 88 juveniles ha–1). At an
individual-level, the water stress (estimated from leaf δ13C) of yew juveniles seems alleviated by the crown cover by neighbors
while it increases with the basal area of conifers. Yew conservation should focus on selective felling for the reduction of basal area
of neighbors surrounding the target tree, but avoid affecting the canopy cover to contribute to enhanced yew juvenile growth.
Keywords: Biodiversity conservation; δ13C; forest management; plant-plant interaction; recruitment; Taxus baccata; water use
efficiency.
Citation: Casals, P., Camprodon, J., Caritat, A., Rios, A.I., Guixé, D., Garcia-Marti, X., Martín-Alcón, S., Coll, L. (2015). Forest
structure of Mediterranean yew (Taxus baccata L.) populations and neighbor effects on juvenile yew performance in the NE Iberian
Peninsula. Forest Systems, Volume 24, Issue 3, e042, 10 pages. http://dx.doi.org/10.5424/fs/2015243-07469.
Supplementary material: This work has 1 supplementary table and 1 supplementary figure published online alongside the
electronic version of the article.
Received: 01 Feb 2015. Accepted: 11 Sep 2015
Copyright © 2015 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution-Non
Commercial (by-nc) Spain 3.0 Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original work is properly cited.
Funding: This work was developed in the frame of the Life Taxus project (LIFE+11 NAT/ES/711) funded by the European
Commission. The first author (PC) is financially supported by a Ramón y Cajal contract (Ministerio de Economía y Competitividad,
Spain).
Competing interests: The authors have declared that no competing interests exist.
Correspondence should be addressed to Pere Casals: pere.casals@ctfc.cat
Introduction
Yew (Taxus baccata L.) is a European temperate
species (Preston & Hill, 1997), widely distributed in
regions with mild winters and high humidity. When
climatic conditions become limiting factors, such as
Pere Casals; Jordi Camprodon, Antònia Caritat, Ana I. Ríos, David Guixé, Xavier Garcia-Martí, Santiago Martín-Alcón and Lluis Coll
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
2
system; but roots penetrating deeply into the fissures of
limestone and chalk pavements have been described in
Irish yew woods (Kelly, 1981). In dense Mediterranean
evergreen woodlands, the competition for soil water may
be severe between yew plants and other species, such as
pines or oaks, that present a higher ability to extract
water at lower potentials (e.g. Martínez-Vilalta et al.,
2014). In summary, water stress in yew trees may
mostly depend on the net balance between the competi-
tion for soil water with neighbors and the facilitation by
the same neighbors’ cover, which may reduce the over-
all evaporative demand. These effects may be espe-
cially relevant in the juvenile stage, whether or not they
allow for the plants’ transition to adult status.
The aim of this study is twofold, first, to analyze the
structure of forest with yew in the North-Eastern region
of the Iberian Peninsula at a regional scale. Then, at an
individual scale, it attempts to analyze the role of the
surrounding woody neighbors in the performance of
the yew juveniles. Specifically, it was hypothesized
that in mixed Mediterranean forest, (1) high-density
neighbors may negatively affect the growth of juvenile
yews, but (2) the effect of moderately dense neighbors
covering yew crowns may attenuate the negative effects
of water deficit on yew performance.
Material and Methods
Study area and study sites
The work involves yew populations of the NE Iberian
Peninsula (40°34’ to 42°26’N and 0°10’ to 3°10’E;
Figure 1). In this region, three main physiographic units
can be distinguished: the Pyrenean ranges in the North,
the Coastal ranges bordering the Mediterranean Sea and
the interior Catalan depression belonging to the Ebro
geomorphologic formation. Altitude distribution ranges
from sea level up to 3,000 m a.s.l., with an average alti-
tude of 700 m. The dominant climate is Mediterranean
with a wide array of local microclimates, varying with
altitude and topography. In the foothills of the Pyrenees
and on the northern aspect of the Mediterranean Coastal
ranges, Submediterranean conditions were also common,
according to the definition assigned by Ozenda (1994) as
the area with climatic characteristics between those of
typically Mediterranean and temperate European climate
area (see Sánchez de Dios et al., 2009 for further details).
In the NE Iberian Peninsula, and similarly in other Med-
iterranean regions in Europe, traditional forest activities
were abandoned during the second half of the last cen-
tury, leading to increased forest density (Lasanta-Martin-
ez et al., 2005, Ameztegui et al., 2010) especially in the
Coastal range, with multi-stemmed stump structures.
variety of forest communities (Cortés et al., 2000;
Piovesan et al., 2009). Mediterranean yew stands were
probably isolated into small populations during the last
glaciations (Bennet et al., 1991) and are now endan-
gered by current land-use changes and fire spread.
Hence, the Mediterranean yew habitat is recognized as
a priority habitat for biodiversity conservation within
the European Union (Habitat 9580*, European Council
Directive 43/92/EEC, European Commission, 1992).
Facilitation among plants occurs when the recruitment
and survival of one species is enhanced by another spe-
cies by making the physical environment under its
canopy more suitable for the beneficiary (Bertness &
Callaway, 1994; Verdú & García-Fayos, 1996; Garcia
et al., 2000). However, the net result of plant interactions
may depend on the stress induced by the direct environ-
ment, which could be positive in some conditions but
become negative under others (Iskulo et al., 2012). The
need to identify appropriate management to maintain or
enhance the resilience of forest ecosystems under the
projected impacts of climate change has been high-
lighted by different authors (e.g. Lindner, 2000; Messi-
er et al., 2013; Coll, 2014). From a conservation point
of view, the identification of facilitation mechanisms
may be useful for the management of threatened plants,
such as the yew, or for the enhancement of the resilience
of ecosystems to the projected impacts of the climate
change (e.g. Batllori et al., 2009).
Although yew is an extremely shade-tolerant species
(Niinemets & Valladares, 2006), the competition for light
has been indicated as the main factor in explaining the
decline of yew populations under a dense canopy (Rupre-
cht et al., 2009; Schwendtner, 2011). Recently, Devaney
et al. (2015) reported a reduced number of juvenile yews
in shade conditions in the southwest Ireland and sug-
gested that light availability may be a limiting factor in
the recruitment of yew to later demographic stages. How-
ever, some discrepancies may be found in the literature
examining light responses in controlled environments.
Hence, whereas Iszkulo & Boratyński (2006) showed that
yew plants are able to establish under extremely dark
conditions, with less than 2% photosynthetic photon flux
density, but cannot grow to adult size, Perrin & Mitchell
(2013) under experimental light conditions did not find
mortality of yew saplings at heavy shade (<3% day-light).
In Mediterranean conditions, while a shortage of light can
compromise the survival of seedlings, juvenile yews may
take advantage of growing in slight shade which provides
a reduction of evaporative demand during drought periods.
Yew is a medium drought-tolerant species (Niinemets
& Valladares, 2006). It usually grows in localities with
a mean annual rainfall higher than 600 mm, though
optimally being around 850 mm. The yew root system
is mostly superficial, with an extensive horizontal root
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
3
Neighbors’ structure and juvenile yew
46 localities, widely distributed in both Pyrenean and
Costal ranges, between 300 and 1600 m a.s.l. (Figure 1).
Stand structural attributes
To ensure that the study cover the entire habitat area,
the structure of yew stands was inventoried in a total of
55 plots distributed over 14 sites in the NE Iberian Pen-
insula (Figure 1, Table 1). Sites were systematically se-
lected to include the main distribution areas of the yew
habitat: five were located in the Southern foothills of the
Pyrenees; another four and five in the northern and south-
ern coastal ranges, respectively (Figure 1). In each site,
and according to the area of the yew population, between
1 and 17 plots were randomly placed for analyzing the
structure of forest with yew (Table S1 [online supple-
ment]). In each site, plots were selected based on the
density of yew trees. Circular inventory plots had an 8 m
radius, except in the Mediterranean sites of Capçanes and
Colldejou (LLCA and LLCO), where the radius was 5 m
due to high stem density. In each plot, we recorded the
species name and the diameter of all trees at breast height
(1.3 m), greater than 7.5 cm. These measures were used
to estimate stand over story variables: stocking density
(stems ha–1 with dbh>7.5 cm), basal area (m2 ha–1), mean
diameter (dbh_mean, cm), the distribution of basal area
into three diameter classes: fine wood (FW, 7.5 cm <dbh<
17.5 cm), medium wood (MW, 17.6 cm <dbh <27.5 cm)
and thick wood (TW, dbh> 27.5 cm) and the contribution
to the stand basal area of five species groups: yew, pines,
oaks, beech, and other broadleaved trees. In each plot we
also recorded the number of yew recruits (dbh<2.5 cm)
and juveniles (7.5 cm >dbh> 2.5 cm).
In the study region, yew is largely distributed in the
mountain ranges along the coast and the meridian foot-
hills of the Pyrenees. In these ranges, yew has naturally
established and grows in small isolated groups in ravines
and on cliffs or as a sub-canopy tree in mixed forests
dominated by pines (Pinus nigra ssp salzmanii (Dunal)
Franco, P. sylvestris L.) or oaks (Quercus pyrenaica
Willd., Q. pubescens Willd.) with other deciduous trees
(Sorbus aria (L.) Crantz, Acer sp.pl.). Although yew
grows mostly on calcareous lithologies it can be also
found growing on acidic rocks in the northern coastal
range. The habitat of yew (9580*) has been mapped in
Table 1. Geographic characteristics of localities with yew populations in the NE Iberian Peninsula
Ref Locality Region Long. Lat. Altitude
m a.s.l.
Annual
rainfall1
mm
Mean
temp1
°C
Climate
Region2
AGLL Llongarriu Pyrenees 2°26’ 42°15’ 695-705 1100-1150 11-12 Submed
AGMC Miseclòs Pyrenees 2°31’ 42°14’ 360-365 950-1000 13-14 Submed
AGOR Orri Pyrenees 2°38’ 42°16’ 915-920 1050-1100 11-12 Submed
MNTS Montsec Pyrenees 0°51’ 42°02’ 1380-1385 750-800 12-13 Submed
SORS Ribera Salada Pyrenees 1°26’ 42°05’ 870-880 750-800 11-12 Submed
LLCA Capçanes South. costal r. 0°48’ 41°04’ 557-586 550-600 14-15 Med
LLCO Colldejou South. costal r. 0°51’ 41°05’ 644-774 600-650 14-15 Med
MOPC Pla Calma North. costal r. 2°20’ 41°46’ 1093-1275 950-1000 8-9 Mid-Temp
MOTH Turó Home North. costal r. 2°26’ 41°46’ 1504-1529 1000-1050 6-7 Mid-Temp
OSCE Centelles North. costal r. 2°12’ 41°45’ 805-838 700-750 12-13 Submed
OSSA Savassona North. costal r. 2° 20’ 41°57’ 650-680 950-1000 12-13 Submed
POPE La Pena South. costal r. 1°04’ 41°21’ 950-1000 650-700 12-13 Submed
POTI Titllar South. costal r. 1°00’ 41°19’ 990-1000 650-700 10-11 Submed
RASQ Rasquera South. costal r. 0°35’ 40°57’ 700-750 650-700 14-15 Med
1 Climatic variables were estimated using a georeferenced model (Ninyerola et al. 2000); http://territori.gencat.cat/ca/atles_climatic/02/.
2 Climate regions dened following the temperature and rainfall criteria of Sánchez de Dios et al. (2009).
Figure 1. Location of the studied yew populations (stars) and
the known forests with yew localities (dots) in Catalonia, NE
Iberian Peninsula. The characteristics of studied sites are de-
scribed in Table 1.
Pere Casals; Jordi Camprodon, Antònia Caritat, Ana I. Ríos, David Guixé, Xavier Garcia-Martí, Santiago Martín-Alcón and Lluis Coll
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
4
Juvenile yew characteristics and structure
of the neighbors
The effect of surrounding woody neighbors on ju-
venile yews was studied in 103 circular plots distrib-
uted in 5 of the 14 previously inventoried sites. These
5 sites corresponded to the mixed forest typologies
defined by a cluster analysis based on the stand struc-
ture characteristics (see results section). A total of 67
plots were placed in the two Mediterranean sites
(LLCA, LLCO) and the rest of the plots (35) in the
three Submediterranean sites (AGOR, POPE, POTI).
The plots were randomly located within each site
but spaced at least 25 m apart. Each circular plot (3 m
radius) was centered with one juvenile (7.5 cm >dbh>
2.5 cm), which was characterized by its dbh, height
and maximum and normal crown diameters. In each
yew, three branches located in the upper, southernmost
part of the crown were measured to determine the
length of the last two years’ twig growth. At least three
twigs were also cut from the upper-part of the crown
of each yew to later separate, in the lab, at least 30 one
year-old leaves which would be used to analyze the
13C:12C abundance isotope ratio (δ13C). This ratio has
been used to investigate the relative water use effi-
ciency (WUE) over extended periods (e.g. Donovan &
Ehleringer, 1994, Lloret et al., 2004). We assumed that
the growth status of juvenile yews may be estimated
by the WUE efficiency measured from the δ13C of the
last year’s leaves and the growth of the last two years
determined from twigs measured in three canopy
branches. The structure of neighbors was characterized
by recording the species name and the dbh of all woody
plants (dbh>1 cm) growing in the 3 m radius plot sur-
rounding each yew. These measures were used to esti-
mate the basal area of neighbors (cm2 m–2), which was
subsequently classified into conifer, deciduous or ev-
ergreen functional groups. In each plot, we visually
estimated the percentage of the yew crown covered by
trees. To estimate total canopy cover, the percentage
of all species was added together.
Statistical analysis
The 55 inventoried yew populations were classified
into different structural typologies using a Ward’s hi-
erarchical cluster with the squared Euclidean distance
method on the variables indicated in Table 2 (except
total and yew densities and other broadleaf or thick
wood basal area proportions). Differences in the den-
sity of yew recruits or juveniles, characteristics of yew
Table 2. Structural stand variables1 for each forest typology obtained by the cluster analysis2, interpretation and locality refer-
ences3 belonging to each group. Mean and standard error indicated between parentheses. The number of stands in each typology
is indicated (n)
T1
n=24
T2
n=15
T3
n=8
T4
n=8
Tree density stems ha–1 1564 (165) 2047 (304) 1386 (156) 596 (96)
Yew density stems ha–1 291 (59) 75 (21) 839 (103) 307 (76)
Basal area (G) m2 ha–1 40.3 (2.6) 24.9 (3.6) 31.0 (4.3) 45.4 (5.3)
dbh mean cm 19.0 (0.9) 12.4 (0.5) 16.7 (0.4) 33.1 (2.9)
dbh CV % 56.0 (2.7) 30.0 (2.8) 41.0 (2.2) 69.1 (6.9)
Taxus b. %G 15.4 (3.0) 6.3 (4.7) 63.1 (2.9) 83.6 (5.6)
Pinus sp. %G 42.7 (5.7) 9.1 (3.6) 8.7 (5.0) 8.0 (5.5)
Quercus %G 26.5 (4.3) 62.8 (6.6) 22.0 (5.1) 4.9 (1.9)
Fagus %G 6.8 (4.7) 0.0 (0.0) 0.0 (0.0) 2.5 (1.7)
Other broadleaf %G 8.7 (2.7) 21.8 (4.6) 6.2 (4.5) 0.9 (0.7)
Fine wood %G 28.4 (3.2) 79.9 (4.6) 35.3 (1.6) 7.5 (1.4)
Medium wood %G 19.1 (2.2) 18.8 (4.8) 44.2 (5.2) 9.7 (3.9)
Thick wood %G 52.5 (3.0) 1.2 (1.2) 20.5 (5.5) 82.8 (5.0)
Forest structure
interpretation
Mixed pine, oak
forests with yew
Mixed dense broadleaf
forest with yew
Yew groves with
oak trees
Mature yew
groves
Locality reference3AGLL LLCA LLCA AGMC AGOR
AGMC LLCO LLCO OSCE MOTH
AGOR OSSA MOTH SORS RSQA
MOPC POPE POPE MNTS
MOTH POTI POTI
1 Structural variables of woody plants with dbh>7.5 cm.
2 All the variables were used in the cluster analysis except total or yew densities, other broadleaf or thick wood basal area proportions.
3 The characteristics for each locality reference are described in Table 1.
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
5
Neighbors’ structure and juvenile yew
tribution to the total basal area of the stand, less than
20% (Table 2). In contrast, in the other two groups (T3
and T4) more than half of the total basal area corre-
sponded to yew trees. The stands belonging to the
T3 group corresponded to a dense forest, with the low-
est basal area and a dominance of fine wood, while the
T4 stands had the lowest stocking density but the high-
est basal area and a dominance of thick wood (Table 2).
About three quarters of the inventoried stands (71%)
were classified into the first two groups, which included
stands from both Costal range and Pyrenean localities
(Table 2).
Yew recruitment reached from nil to 4,129 recruits
ha–1 and 1,019 juveniles ha–1 (mean ± SE: 625 ± 104
recruits ha–1, 259 ± 55 juveniles ha–1; Suppl. Table
S1 [online supplement]). The number of recruits and
juveniles in the stands belonging to the T4 group was
clearly lower than in the rest of typologies (Table 3).
Moreover, only three stands of the total eight in this
group had recruits (Table 3). Since the percentage
of juveniles respect to the number of recruits stand
by stand was calculated only for those plots with
regeneration (n=3 in the T4 group), we did not find
significant differences in the ratio between typolo-
gies (Table 3).
Juveniles’ yew growth and structure
of neighbors
The individual basal area of the 103 studied juvenile
yews spanned from 5.0 cm2 to 43.0 cm2 and the height
from 0.3 m to 6.0 m (Table 4). Both basal area and
height of juveniles were higher in Submediterranean
localities than in Mediterranean ones. The yearly
growth length of twigs during the last two years ex-
tended from less than 1 cm y–1 to 9.8 cm y–1, and the
δ13C from -33.37 ‰ to -28.05 ‰. No differences were
detected in any of these two variables between regions
(Table 4).
juveniles or neighbor structure variables between the
obtained structural types were analyzed by One-way
ANOVA. Multiple linear regressions were used to relate
the juvenile yew twig growth or WUE with the neigh-
bors’ structural and compositional variables. Step-wise
method was used to select the significant variables in
the regression model. Model residuals distribution and
spatial autocorrelation were tested by graphs and the
Durbin-Watson test. Data used in the ANOVA and
linear regressions was tested for normality and homo-
scedasticity and log-transformed if necessary. Statisti-
cal analyses were performed using SPSS v.20.
Results
Structural characterization of forest stands
with yew
The inventoried 55 forest stands with yew trees were
mostly located on north facing aspects (74% of stands
in N, NE or NW), with slopes ranging from 10° to 45°
and altitudes extending from 360 m to 1,529 m a.s.l.
(Table S1 [online supplement]). Annual rainfall in the
forest localities with yew ranges from 600 mm to 1,100
mm and mean annual temperature from 6°C to 15°C
(Table 1). Total stocking density expanded from 149
stems ha–1 to 4,584 stems ha–1 and the total basal area,
from 0.85 m2 ha–1 to 75.6 m2 ha–1 (Table S1 [online sup-
plement]). The proportion of yew basal area to total
stand basal area extends from less than 1% to 99.6%
(Table S1 [online supplement]). A cluster analysis clas-
sified the 55 stands into four structural typologies
(Table 2). The cut-off point of the cluster corresponded
to a sharp increase in the linkage distances in clustering
steps (Fig. S1 [online supplement]). Two forest types
(T1 and T2) corresponded to multi-stratified forests,
dominated either by pine and oak trees (T1) or other
broadleaved tree species (T2) with scattered presence of
yew. In these types, yew represented only a minor con-
Table 3. Number of yew adults (dbh > 7.5 cm), juveniles (7.5 cm > dbh > 2.5 cm) and recruits (dbh < 2.5 cm) and the proportion
of juveniles vs recruits for each forest typology obtained by the cluster analysis. The number of stands in each typology is indi-
cated (n). Mean and standard error between parentheses. The signicance of One-way ANOVA was shown. For each variable,
different letters indicate differences between forest typologies
T1
n=24
T2
n=15
T3
n=8
T4
n=8
Signicance
p-valor
Adults nº ha–1 291 (59) a 75 (21) b 839 (103) c 307 (76) a 0.001
Juveniles nº ha–1 340 (114) a 253 (48) a 292 (119) a 57 (17) b 0.016
Recruits nº ha–1 849 (213) a 622 (130) a 373 (117) ab 181 (88) b 0.029
Juv : Recr % 80 (17) 63 (19) 77 (29) 28 (15) 0.810
T1. Mixed pine, oak forests with scattered yews; T2. Mixed dense broadleaf forest with yew; T3. Yew groves with oak trees; T4. Mature
yew groves.
Pere Casals; Jordi Camprodon, Antònia Caritat, Ana I. Ríos, David Guixé, Xavier Garcia-Martí, Santiago Martín-Alcón and Lluis Coll
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
6
bors were higher in the Mediterranean plots than in
Submediterranean ones. Among functional groups, the
basal area of deciduous and evergreen neighbors was
also higher in the Mediterranean plots, while no differ-
ences were found in the basal area of conifers (Table 4).
Yearly twig length growth and δ13C did not correlate
(r=0.04, p=0.718, n=103). Twig length growth did not
show any relationships with any neighbors’ measured
variable. The multiple regression model showed that
leaf δ13C of yew juveniles decreased with the percent-
age of yew crown covered by neighbors and increased
with the basal area of conifers (log-transformed) (Fig-
ure 2, Table 5). Basal areas of the evergreen or de-
ciduous functional groups were excluded from the
model. Adding the region into the model (as a dummy
variable) increased the explained part of the δ13C
variability from 14.5% to 17.0%; a change which was
significant (p=0.048). This dummy variable shifted
the equation upwards or downwards by modifying the
constant (k, Table 5) and indicated higher δ13C in the
Mediterranean than in the Submediterranean region.
Discussion
In the NE Iberian Peninsula, the habitat of yew has
been mapped mostly in northward facing forest stands,
widely distributed through the coastal range and the
Table 4. Characteristics of yew juveniles and of the forest structure of neighbors growing in a 3m radius plot centered in the
yew in Mediterranean and Submediterranean regions. Mean, standard error between parentheses, maximum and minimum. The
signicance of the difference between localities is indicated for each variable
Mediterranean (n=68) SubMediterranean (n=35) Signif.
Mean SE Max Min Mean SE Max Min p-valor
Yew Juvenile 1
Basal area cm 15.6 (1.5) 43.0 5.0 28.4 (1.4) 44.2 10.5 0.001
Height cm 290 (18) 550 34 409 (16) 600 197 0.001
Crown diam. cm 105 (17) 437 15 337 (19) 648 20 0.001
Leaf δ13C ‰ –30.7 (0.1) –28.0 –33.4 –30.9 (0.2) –29.4 –33.1 0.415
twig length cm 4.0 (0.2) 7.3 0.1 3.8 (0.3) 9.8 0.0 0.436
Neighbors structure2
Yew crown cover3%119 (6) 260 5 92 (6) 180 0 0.010
Total basal area cm m–2 52.7 (4.6) 190.0 0.0 36.6 (5.2) 114.8 0.1 0.033
Conifer basal area4cm m–2 18.7 (3.9) 182.0 0.0 20.3 (4.8) 83.0 0.0 0.760
Deciduous b.a.4cm m–2 8.0 (1.5) 71.0 0.0 5.5 (3.3) 113.0 0.0 0.007
Evergreen b.a.4cm m–2 26.1 (2.8) 132.0 0.0 10.8 (2.0) 52.0 0.0 0.001
1 Crown diam. Mean between maximum and normal crown diameters; Twig length. Median of the annual growth of the two last years
of three crown branches; δ13C. Isotope C abundance ratio of one-year old yew leaf collected from at least three crown branches.
2 The structural variables of neighbors were recorded in all the woody species with dbh >1 cm.
3 Proportion of yew crown covered by neighbor crowns. The values are higher than 100 as they are calculated as the sum of different
neighbors crowns.
4 Total, conifer, deciduous and evergreen basal area of woody species of each group growing in the 3 m radius plot.
Figure 2. Predicted δ13C (‰) of juvenile yew along the propor-
tion of yew crown covered by neighbours (%) and the basal area
of conifer neighbors (Log-transformed, cm m–2) according to
regression model in Table 5 (Region dummy variable was set
as 0). To reect the layering of the cover of the yew crown
cover by neighbors, the canopy percentage cover of each species
was summed up.
–29.5
–30.0
–30.5
–31.0
–31.5
–32.0
–32.5
200 150 100 50 0
200
150
100
50
0
–29.0
Crown Cover (%)
Conifer Basal Area (cm
2
m
–2
)
13C‰
The forest structure surrounding the yew juveniles
was different between regions (Table 4). Both the pro-
portion of the juvenile yew crown covered by other
woody species and the total basal area of woody neigh-
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
7
Neighbors’ structure and juvenile yew
southern foothills of the Pyrenees, in a wide range of
altitudes (between 300 – 1,600 m a.s.l.) and in Mediter-
ranean or Submediterranean bioclimatic regions (Font,
2014 and unpublished data). In these conditions, yew
is found in a wide spectrum of forest structures, from
clear stands to dense forests as indicated by the total
stocking density (ranging from 149 stems ha–1 to 4,584
stems ha–1) and the total basal area (ranging from
0.85 m2 ha–1 to 75.6 m2 ha–1).
In general, the density of recruits and juveniles
(625 ± 104 recruits ha–1, 259 ± 55 juveniles ha–1) found
in the monitored stands was higher than the ones re-
ported in other Mediterranean forests in which yew
appears (e.g. García et al., 2000; but see Farris & Fi-
ligheddu, 2008) and similar to those from more temper-
ate European areas (Hulme, 1996; García & Obeso,
2003; Dhar et al., 2006; Piovesan et al., 2009). How-
ever, and similar to other regions, the recruitment of
yew is low or nonexistent in yew dominated stands
(181±88 individuals ha–1). In Mediterranean localities
and under these conditions, low yew recruitment may
be explained, at least partially, by (i) severe droughts
(ii) high seed-predation rates (Sanz & Pulido, 2014),
(iii) high browsing pressure caused by herbivores due
to the absence of the protection of nursery plants (sensu
Garcia & Obeso 2003; Mendoza et al., 2009) and (iv)
the extremely dark conditions under the canopy of the
mature yews (Iszkulo & Boratyński, 2006; Perrin et al.,
2006).
Light is one of the main factors structuring forests
and affecting the composition of species. In Mediter-
ranean climate areas, where water supplies vary intra-
and inter-annually, the plant water stress has also an
important role in structuring the forests. When water
is limited, adjacent plants may compete for soil water.
In such cases, the competitive advantage of one species
over another is triggered by the capacity to extract
water from the soil at lower potential or the capacity
to reduce the water losses by evapotranspiration. Drier
conditions increase the WUE of plants, which culmi-
nates in higher δ13C values of plant tissues (e.g. Dono-
van & Ehleringer, 1994, Lloret et al., 2004). Hence,
higher δ13C values in leaves of adult yews (data not
shown) compared with those in juveniles growing in
the same Mediterranean sites suggest that adults are
more water-stressed than young ones. Although no dif-
ferences in δ13C were detected among juvenile yews
growing in Mediterranean or Submediterranean lo-
calities, the regression model predicts that Mediterra-
nean juveniles were more water stressed than Sub-
mediterranean ones. Even though other factors related
with micro-site characteristics (e.g. soil depth) can also
modulate the observed patterns, our results indicated
that the yew juveniles benefit from the canopy of neigh-
bors covering yew crowns. The cover of yew by the
neighbors’ crowns probably reduces the evapotranspi-
ration of juvenile yew during periods with high atmos-
pheric evaporation demand. However, a negative effect
was found when the density and size of neighbors
growing close to the yew juveniles is too high, likely
due to an increase in the competition for soil water
between the yews and the other woody species.
Management practices such as traditional selective
thinning of Mediterranean oak coppices have been dem-
onstrated to reduce the consequences of long drought
periods compared with unthinned plots (Cotillas et al.,
2009). However, it is worth highlighting that these au-
thors also stated that the intensity and frequency of this
management should be considered to ensure the effi-
cacy of the treatments and to avoid non-desired effects.
In Slovakia, for example, Saniga (2000) found that a
reduction of around 18-20% of volume in the surround-
ing density in a stand dominated by Fagus and Picea
abies improved the height growth of yew, whereas a
reduction by 7-8% resulted in no growth above the con-
trol plots (cited in Thomas & Polwart, 2003).
In conclusion, the lack of yew recruitment in dense
mature forest and the juvenile performance in less
dense structures may constrain yew conservation in the
midterm. As water availability in the Mediterranean
region is likely to decrease in the near future (IPCC,
2013) and forest densification is expected to continue
Table 5. Multiple linear regression stepwise model (y=k+ax1+bx2+cx3) between the δ13C of juvenile yew and the region, the
proportion of yew crown covered by neighbors (%) and the basal area of conifer neighbors (log-transformed conifer G). For
each independent variable the standard error of each parameter is shown in parenthesis and the statistical signicance by (*)
p<0.05, (**) p<0.01, (***) p<0.001. The adjusted coefcient of determination (adjusted r2) and the signication (p-value) of
the model is indicated
Parameters Signication
k Region1Cover conifer G (log) adj r2p-valor
Leaf δ13C (‰) –29.91 (0.28) *** –0.43 (0.21) * –0.01 (0.01) *** 0.32 (0.12) ** 0.17 0.001
1 Region dummy variable: 0. Mediterranean; 1. Submediterranean.
Pere Casals; Jordi Camprodon, Antònia Caritat, Ana I. Ríos, David Guixé, Xavier Garcia-Martí, Santiago Martín-Alcón and Lluis Coll
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
8
to rise, selective cuttings addressing the reduction of
basal area of neighbors surrounding the target yew
should be promoted since they may increase soil mois-
ture and encourage juvenile growth. However, it would
be suggested that removing neighboring woody plants
be done with care in order to prevent excessive expo-
sure of the juvenile yew crown to light. As other factors
at the tree scale may be relevant, further studies should
focus on the thresholds of thinning management.
Acknowledgments
We wish to thank everyone who was involved in this
project, and especially Jarkov Reverté, Xavier Bu-
queras, Roman Borràs, Sara Sánchez, Sonia Navarro,
Sílvia Busquet, Guillem Argelich, Victor Aguilà and
Carme Casas.
References
Ameztegui A, Brotons L, Coll L, 2010. Land-use changes as
major drivers of mountain pine (Pinus uncinata Ram.)
expansion in the Pyrenees. Glob Ecol Biogeogr19: 632-
641. http://dx.doi.org/10.1111/j.1466-8238.2010.00550.x.
Batllori E, Camarero JJ, Ninot JM, Gutiérrez E, 2009. Seedling
recruitment, survival and facilitation in alpine Pinus unci-
nata treeline ecotones. Implications and potential respons-
es to climate warming. Glob Ecol Biogeogr 18: 460-472.
http://dx.doi.org/10.1111/j.1466-8238.2009.00464.x.
Bennett KD, Tzedakis PC, Willis K.J, 1991. Quaternary
refugiaof north European trees. Journal of Biogeography
18: 103-115. http://dx.doi.org/10.2307/2845248.
Bertness M, Callaway RM, 1994. Positive interactions in
communities. Trends Ecol Evol 9: 191-193. http://dx.doi.
org/10.1016/0169-5347(94)90088-4.
Coll L, 2014. Gestión selvícola y regeneración natural ante
un futuro incierto: marco teórico y principios generales.
Cuadernos de la SECF 40: 19-32.
Cortés S, Vasco F, Blanco E, 2000. El libro del tejo. Arba,
Madrid (España). 336 pp.
Cotillas M, Sabaté S, Gracia C, Espelta JM, 2009. Growth
response of mixed Mediterranean oak coppices to rainfall
reduction. Could selective thinning have any influence on
it? For Ecol and Manage 258: 1677-1683.
Devanay JL, Whelan PM, Jansen MA, 2015. Light respons-
es of yew (Taxus baccata L.); does size matter?. Trees,
29:109-118. http://dx.doi.org/10.1007/s00468-014-1095-x.
Dhar A, Ruprecht H, Klumpp R, Vacik H, 2006. Stand struc-
ture and natural regeneration of English yew (Taxus bac-
cata L.) at Stiwollgraben in Austria. Dendrobiology 56:
19-26.
Donovan LA, Ehleringer Jr, 1994. Carbon isotope discrimi-
nation, water-use effciency, growth, and mortality in a
natural shrub population. Oecologia 100: 347-354. http://
dx.doi.org/10.1007/BF00316964.
European Commission, 1992. Council Directive 92/43 EC
of July 22. Official Journal of the European Union L 206
22/7/1992. pp 7-50.
Farris E, Filigheddu R, 2008. Effects of browsing in relation
to vegetation cover on common yew (Taxus baccata L.)
recruitment in Mediterranean environments. Plant Ecol
199: 309-318. http://dx.doi.org/10.1007/s11258-008-
9434-x.
Font X, 2014. Mòdul Flora i Vegetació. Banc de Dades de
Biodiversitat de Catalunya. Generalitat de Catalunya i
Univ. de Barcelona. http://biodiver.bio.ub.es/biocat/.
Garcia D, Obeso JR, 2003. Facilitation by herbivore-meditated
nurse plants in a threatened tree, Taxus baccata: local effects
and landscape level consistency. Ecography 26: 739-
750. http://dx.doi.org/10.1111/j.0906-7590.2003.03601.x.
Garcia D, Zamora R, Hódar JA, Gómez, JM, Castro J, 2000.
Yew (Taxus baccata L.) regeneration is facilitated by
fleshy-fruited shrubs in Mediterranean environments. Biol
Conserv 95: 31-38. http://dx.doi.org/10.1016/S0006-
3207(00)00016-1.
Hulme PE, 1996. Natural regeneration of yew (Taxus bac-
cata L.): microsite, seed or herbivore limitation? J Ecol
84, 853-861. http://dx.doi.org/10.2307/2960557.
IPCC, 2013. Summary for Policymakers. In: Climate Change
2013, The Physical Science Basis. Contribution of Work-
ing Group I to the Fifth Assessment Report of the Inter-
governmental Panel on Climate Change. (Stocker T F
et al. eds.). Cambridge University Press, Cambridge,
United Kingdom and New York, NY, USA.
Iszkuło G, Boratyński A, 2006. Analysis of the relationship
between photosynthetic photon flux density and natural
Taxus baccata seedlings occurrence. Acta Oecol 29: 78-
84. http://dx.doi.org/10.1016/j.actao.2005.08.001.
Iszkuło G, Didukh Y, Giertych MJ, Jasińska AK, Sobiera-
jska K, Szmyt J, 2012. Weak competitive ability may
explain decline of Taxus baccata. Ann For Sci 69: 705-
712. http://dx.doi.org/10.1007/s13595-012-0193-4.
Kelly DL, 1981. The native forest vegetation of Killarney
south –west Ireland – an ecological account. J Ecology
69: 437-472. http://dx.doi.org/10.2307/2259678.
Lasanta-Martinez T, Vicente-Serrano SM, Cuadrat-Prats JM,
2005. Mountain Mediterranean landscape evolution caused
by the abandonment of traditional primary activities: a
study of the Spanish Central Pyrenees. Appl Geog 25(1):
47-65. http://dx.doi.org/10.1016/j.apgeog.2004.11.001.
Lindner M, 2000. Developing adaptative forest management
strategies to cope with climate change. Tree Physiology 20:
299-307. http://dx.doi.org/10.1093/treephys/20.5-6.299.
Lloret F, Peñuelas J, Ogaya R, 2004. Establishment of co-
existing Mediterranean tree species under a varying soil
moisture regime. J Veg Sci 15: 237-244. http://dx.doi.
org/10.1111/j.1654-1103.2004.tb02258.x.
Martínez-Vilalta J, Poyatos R, Aguadé D, Retana J, Mencuccini
M., 2014. A newlook at water transport regulation in plants.
New Phytol 204: 105-115. http://dx.doi.org/10.1111/nph.12912.
Mendoza I, Gómez-Aparicio L, Zamora R, Matías L, 2009.
Recruitment limitation of forest communities in a de-
graded Mediterranean landscape. J Veg Sci 20: 367-376.
http://dx.doi.org/10.1111/j.1654-1103.2009.05705.x.
Forest Systems December 2015 • Volume 24 • Issue 3 • e042
9
Neighbors’ structure and juvenile yew
Ecol 205: 23-46. http://dx.doi.org/10.1007/s11258-009-
9596-1.
Ruprecht H, Dhar A, Aigner B, Oitzinger G, Klumpp R,
Vacik H, 2009. Structural diversity of English yew (Taxus
baccata L.) populations. Eur J For Res 129: 189-198.
http://dx.doi.org/10.1007/s10342-009-0312-4.
Sánchez de Dios R, Benito-Garzón M, Sainz-Ollero H, 2009.
Present and future extension of the Iberian submediter-
ranean territories as determined from the distribution of
marcecescent oaks. Plant Ecol 204: 189-205. http://dx.doi.
org/10.1007/s11258-009-9584-5.
Saniga M, 2000. Struktfira, produkcn a regeneracne pocesy
tisa obcajneho v Stitnej Prirodnej Rezervaicii Plavno
[Structure, production and regeneration processes of Eng-
lish yew in the State Nature Reserve Plavno]. Journal of
Forest Science, 46: 76-90.
Sanz R, Pulido F, 2014. Post-dispersal seed depletion by
rodents in marginal populations of yew (Taxus baccata):
consequences at geographical and local scales. Plant Spe-
cies Biology 29: 48-54. http://dx.doi.org/10.1111/1442-
1984.12030.
Schwendtner O, 2011. Supervivencia y crisis del tejo (Taxus
baccata L.) en el área cantábrica. II Jornadas del Tejo en
el Mediterráneo Occidental, Olot (España), 26-28 de Julio.
pp. 43-49.
Thomas PA, Polwart A, 2003. Taxus baccata L. J Ecol, 91: 489-
524. http://dx.doi.org/10.1046/j.1365-2745.2003.00783.x.
Verdú M, García-Fayos P, 1996. Nucleation processes in a
Mediterranean bird-dispersed plant.Funct. Ecol. 10: 275-
280. http://dx.doi.org/10.2307/2389853.
Messier C, Puettmann KJ, Coates KD, 2013. Managing for-
ests as complex adaptive systems: Building resilience to
the challenge of global change. Routledge, NY. 368 pp.
Niinemets Ü, Valladares F, 2006. Tolerance to shade, drought,
and waterlogging of temperate Northern Hemisphere trees
and shrubs. Ecol Monographs 76: 521–547. http://dx.doi.
org/10.1890/0012-9615(2006)076[0521:TTSDAW]2.0.
CO;2.
Ninyerola M, Pons X, Roure JM, 2000. A methodological
approach of climatological modelling of air temperature
and precipitation through GIS techniques. Int J Climatol
20: 1823-1841. .
Ozenda P, 1994. Végétation du continent européen. De-
lachaux et Niestlé, Lausanne. Swizerland. 271 pp.
Perrin PM, Mitchell FJG, 2013. Effects of shade on growth,
biomass allocation and leaf morphology in European yew
(Taxus baccata L.). Eur. J For Res, 132:211-218. http://
dx.doi.org/10.1007/s10342-012-0668-8.
Perrin PM, Kelly DL, Mitchell FJG, 2006. Long-term deer
exclusion in yew-wood and oakwood habitats in south-
westIreland: natural regeneration and stand dynamics. For
Ecol Manage, 236:356-367.
Preston CD, Hill MO, 1997. The geographical relation-
ships of British and Irish vascular plants. Botanical
Journal of the Linnean Society, 124, 1-120. http://dx.doi.
org/10.1111/j.1095-8339.1997.tb01785.x.
Piovesan G, Presutti Saba E, Biondi F, Alessandrini A, Di
Filippo A, Schirone B, 2009. Population ecology of yew
(Taxus baccata L.) in the Central Apennines: spatial pat-
terns and their relevance for conservation strategies. Plant
