Trees (2010) 24:463–470
DOI 10.1007/s00468-010-0414-0
ORIGINAL PAPER
Vessel features of Quercus ilex L. growing under Mediterranean
climate have a better climatic signal than tree-ring width
Filipe Campelo • Cristina Nabais • Emilia Gutiérrez
Helena Freitas • Ignacio Garcı́a-González
Received: 13 July 2009 / Revised: 12 January 2010 / Accepted: 18 January 2010 / Published online: 11 February 2010
Ó Springer-Verlag 2010
Abstract We investigated whether vessel time series of
Holm oak (Quercus ilex L.), a diffuse to semi-ring-porous
species, can record a climatic signal which differs from the
signal encoded in tree-ring width (TRW). The study was
conducted in ten Q. ilex trees from a coppice stand in
northeast Spain. Chronologies of TRW, mean vessel area
(MVA) and maximum vessel area (MAX) were developed
and correlated with climate data, for the period 1985–2004
(20 years). Our results indicate that vessel features contain
environmental information that is different from that stored
in TRW. MAX chronologies correlate better to early spring
precipitation (April–May) than TRW chronologies, and so
does MVA of the largest 20–25 vessels from the first third
of the ring with late spring precipitation (May–June). Also,
the combination of MVA and TRW is a better predictor of
summer precipitation. This explorative study clearly shows
that vessel features can complement the climatic signal of
TRW increasing the resolution of the climate reconstruc-
tions for the Mediterranean region.
Communicated by E. Beck.
F. Campelo (&)  C. Nabais  H. Freitas
Centro de Ecologia Funcional, Departamento de Ciências da
Vida, Universidade de Coimbra, 3001-401 Coimbra, Portugal
e-mail: fcampelo@ci.uc.pt
F. Campelo  E. Gutiérrez
Departament d’Ecologia, Facultat de Biologia,
Universitat de Barcelona, Av. Diagonal, 645,
08028 Barcelona, Spain
I. Garcı́a-González
Departamento de Botánica, Escola Politécnica Superior,
Universidade de Santiago de Compostela, Campus de Lugo,
27002 Lugo, Spain
•
Keywords Dendrochronology  Holm oak 
Mediterranean climate  Tree ring  Vessel features
Introduction
Tree rings are used as a biological archive to study past
environmental conditions. The tree-ring width (TRW) is
the anatomical variable traditionally used in dendrochro-
nology, and integrates the prevailing climatic conditions
throughout the growing season and allows the construction
of continuous time series. Since intra-annual climatic
information is difficult to obtain from TRW, other ana-
tomical features have been used to derive signals with a
higher temporal resolution (Wimmer 2002). Among these
are frost rings (LaMarche and Hirschboeck 1984; Brunstein
1996), light rings (Liang et al. 1997; Wang et al. 2000;
Liang and Eckstein 2006), double or false rings (Wimmer
et al. 2000; Masiokas and Villalba 2004; Campelo et al.
2007a) and intra-annual density fluctuations (Bouriaud
et al. 2005; Campelo et al. 2007b; Vieira et al. 2009). The
identification of such anatomical structures in wood is
based on cell characteristics (e.g. wall thickness or lumen
diameter), which are affected by environmental factors
during the process of wood formation (Eckstein 2004;
Fonti et al. 2009b). Studies on several species such as
Quercus macrocarpa Michx. (Woodcock 1989), Fagus
sylvatica L. (Sass and Eckstein 1995), Tectona grandis L.f.
(Pumijumnong and Park 1999), Castanea sativa Mill.
(Fonti and Garcı́a-González 2004) and Prosopis flexuosa
DC (Giantomasi et al. 2009) showed the importance of
climatic conditions on vessel ontogeny.
Obtaining time series of vessel features is highly time-
consuming (Tardif and Conciatori 2006), which may
explain the low number of studies that use vessels as
123
464
ecological or climatological proxies (Fonti et al. 2009a).
The utility of vessel features as potential proxies for den-
droecological studies depends on their capacity to provide
distinct signals or to increase the signal strength of tradi-
tional tree-ring variables (e.g. TRW). Garcı́a-González and
Eckstein (2003) found that the mean vessel area (MVA) in
the earlywood of the ring-porous Quercus robur L. was
strongly correlated to early spring rainfall. Fonti and Gar-
cı́a-González (2008) proposed the use of earlywood vessel
size as a dendroclimatic proxy for mesic sites, where TRW
leads to unsatisfactory results. Most of the studies have
investigated the climatic signal of vessel time series on
ring-porous species (Garcı́a-González and Eckstein 2003;
Fonti et al. 2007) with only a few works in diffuse and
‘‘semi-ring-porous’’ species (Sass and Eckstein 1995).
Quercus ilex L. (Holm oak), an evergreen tree widely
distributed in the Mediterranean area (Terradas 1999), has
a semi-ring to diffuse porous wood anatomy (Schweingr-
uber 1990). It is a drought-tolerant species that can cope
both with frost events during winter and water stress during
summer (Terradas and Savé 1992; Lo Gullo and Salleo
1993; Nardini et al. 2000). There are very few studies
relating vessel features of this species to environmental
conditions in the Mediterranean region (Corcuera et al.
2004), where tree growth is mainly controlled by water
availability (Campelo et al. 2007a, 2009). The size of the
vessels produced along the growing season is a trade-off
between water transportation efficiency and vulnerability
to cavitation. Therefore, one can expect that vessel features
of Q. ilex are strongly controlled by the intra- and inter-
Fig. 1 Study site (open circle)
in the Natural Park of Garraf
and Olèrdola (northeast Spain)
and climatic diagram of the
meteorological station (Begues)
close to the study site. The
dashed line represents
precipitation and the solid line
temperature
[1974-2004]
Mean Temperature (ºC)
30
20
10
0 0
J F M A M J
123
Trees (2010) 24:463–470
annual variability of environmental conditions, namely
water availability during the growing season.
The present study evaluated the potential of vessel
chronologies of Q. ilex to be used as ecological proxies in
the Mediterranean area. The main objectives of this study
were (a) to explore if vessel time series of Q. ilex have a
climatic signal and (b) whether this signal differs from that
enclosed in TRW.
Materials and methods
The study area was located in an interior valley within
Garraf mountains (418200 N, 018500 E, 300 m a.s.l.) in the
Natural Park of Garraf and Olèrdola, northeast of Spain
(Fig. 1). The studied coppice stand resprouted in 1983 after
the fire in 1982 (Campelo et al. 2007a). The vegetation
cover (ca. 95%) is dominated by evergreen, sclerophyllous
shrublands ca. 1.5 m high, and emerging Pinus halepensis
Mill., and Q. ilex up to 5 m high. The climate is Medi-
terranean, with a remarkable dry period in summer (Fig. 1).
A mean annual temperature of 13.4°C and a total annual
precipitation of 659.9 mm, mainly during spring and
autumn, were recorded by the closest meteorological sta-
tion in Begues, located ca. 8 km away from the study area.
Ten Q. ilex trees were felled and cross-sections taken at
a height of 5 cm above ground. One tree was cut in 2004
and the remaining in 2005. The selected trees had a
perimeter at breast height of 15.7 ± 5.8 cm (mean ± SD)
and a height of 3.9 ± 0.9 m (mean ± SD). Cross-sections
1 3 .4 º C 659.9 mm
100
Precipitation (mm)
80
60
40
20
J A S O N D
Trees (2010) 24:463–470 465

were air-dried and sanded with progressively finer grades

of sandpaper (100–800). Cross-sections were visually
crossdated and TRW was measured to the nearest
0.01 mm, across the longest radius, using a Lintab linear
table (Frank Rinn S.A., Heidelberg, Germany). The pro-
gram TSAP (Rinn 2003) was used to check the accuracy of
the visual crossdating.
The ten cross-sections were prepared for vessel mea-
surements. The ground tissue was darkened with NaOH
(Sass and Eckstein 1994) and the tyloses and wood dust
inside the vessels were removed with a high-pressure water
blast. Afterwards, cross-sections were rubbed with white
chalk to fill the open vessels in order to increase the con-
trast between vessel lumen and the ground tissue.
Digital images of the cross-sectional surface were taken
on a radial path from the bark to the pith with a digital
camera (Olympus DP12) attached to a stereomicroscope
(Olympus SZ60). These images were taken along the
radius where TRW was measured. For each ring, a section
([7-mm-width tangential band) was selected using wood
rays and tree-ring limits to establish radial and tangential
boundaries, respectively (Fig. 2). All analyses of the digital
images were performed using ‘‘Image-Pro Plus’’ software
(Media Cybernetics). The minimum vessel lumen area was
set at 250 lm2 (corresponding to a lumen diameter of
18 lm) and the maximum vessel lumen area set at
50,000 lm2 to avoid that objects other than vessels were Fig. 2 Example of Quercus ilex image used to determine the lumen
considered. A shape filter, removing objects whose length vessel area and position within the ring. Each ring is delimited by
was at least twice their width, was also used to exclude thick line in red and vessels are delimited by red contours (thin line).
For each ring, the lumen of the largest vessel is blue and vessels in the
objects of irregular shape. The accuracy of vessel identi-
first third of the ring are yellow
fication was visually confirmed by observation under a
stereomicroscope and when necessary vessels outlines
were manually corrected. For each tree ring, vessel lumen 50

area and the coordinates of its centroid were recorded 30

Vessel lumen area (103 µm2)

(Fig. 2), allowing the determination of the relative radial 20

position (in percentage) of each vessel within a ring 10

(Fig. 3). The MVA and the area of the largest vessel
5
(MAX) were calculated for each ring and for the first third
of the ring. 2.5
Chronologies of TRW and vessel features (MVA and
MAX) were established from individual time series. 1
Growth-related trends were removed from the series by 0.7
0.5
fitting a cubic smoothing spline with a 50% frequency cut-
0.3
off of 32 years (Cook and Peters 1981), and series of
0 10 20 30 40 50 60 70 80 90 100
growth indices were obtained by dividing the original data
Position within the ring (%)
by this function. The same method was applied to all time
series to avoid differences associated with detrending Fig. 3 Variation of the vessel lumen area of all vessels across the
procedures (Garcı́a-González and Eckstein 2003) and to ring; red line shows the smoothing curve using a span width of 0.70
allow the comparison of their climatic signals. The
obtained growth indices were then averaged to produce signal, and expressed population signal (EPS). The EPS
mean growth chronologies using a biweight robust mean. value determines how well a chronology based on a finite
Chronology quality was assessed using correlation between number of trees approximates the theoretical population
trees (Rbt), as a measure of the strength of the common chronology (Wigley et al. 1984). Mean sensitivity (MS)

123
466
and first-order autocorrelation coefficient (AutoR) were
calculated for each standard chronology. For the period
1985-2004, growth variables (TRW, MVA and MAX)
were compared with each other using two-tailed simple
linear correlation (Pearson’s correlation coefficient).
Climate–growth relationships were investigated using a
simple correlation with monthly and monthly grouped total
precipitation and mean air temperature variables. The
contribution of large vessels to the climatic signal of MVA
was achieved by progressively retaining only the n largest
vessels (MVA[n=1:30], where n varies from 1 to 30) and
recalculating chronologies and climate–growth relation-
ships (for more details, see Garcı́a-González and Fonti
2006). In addition, the correlations between precipitation in
April–May, May, May–June and the MVA of the largest n
vessels in whole ring (MVA[n]) and in the first third of the
ring (1/3MVA[n]) were compared, where MVA[1] is equal
to MAX and 1/3MVA[1] is the largest vessel in the first
third of the ring (1/3MAX).
Results
The vessel area ranged from 374 lm2 (ca. 22 lm diameter)
to 38,900 lm2 (ca. 222 lm diameter), with a mean value of
3,729 lm2 (ca. 69 lm diameter). The largest vessel
observed had a lumen diameter 10 times greater than the
smallest vessel. The lumen area distribution frequency of
all measured vessels (n = 22,231) was clearly skewed to
the left, with only a few large vessels (Fig. 4). In fact, more
than half of the vessels (52.7%) showed a lumen area
smaller than 3,000 lm2 and only 5% were larger than
10,000 lm2.
Larger vessels were more frequent in the first third of the
ring while small vessels were found throughout the whole
ring, but more frequent at the end of the ring (Figs. 2, 3). In
the first third of the ring, 1/3MVA and 1/3MAX showed
40
30
% of total vessels
20
10
0 more than 20 vessels. For the precipitation in May-June,
<2 2-4 4-6 6-8 8-10 10-12 12-14
Vessel lumen area class (103 µm2)
Fig. 4 Frequency distribution of vessel area classes for Quercus ilex
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Trees (2010) 24:463–470
mean values of 5,462 and 11,342 lm2, respectively. An
increasing trend in MVA and MAX was initially observed
with cambial age. These vessel features stabilized when
cambial age reached ca. 10 years (Fig. 5).
TRW showed the highest Rbt, MS, AutoR and EPS
values (Table 1). EPS values for MVA and MAX were
slightly lower than the critical value of 0.85 proposed by
Wigley et al. (1984). The MVA chronology showed the
lowest value of first autocorrelation. For the period 1985–
2004, MAX was correlated to TRW (r = 0.73; P \ 0.001)
and MVA (r = 0.59; P \ 0.01), while MVA was not
correlated to TRW (r = 0.07; P = 0.783).
TRW was positively correlated with May and August
rainfall (Fig. 6), negatively correlated with temperature in
September and October and positively with temperature in
November. The only significant relationship between cli-
mate and MVA was obtained for August precipitation of
the previous year. According to McCarroll et al. (2003),
when two proxy variables are controlled by the same
climatic factor, the signal may be enhanced by their
combination. A simple way to test the effectiveness of
combining TRW and MVA to estimate August precipi-
tation is to use both variables independently to predict
precipitation in August (inverse calibration), and then
average the results, with each variable weighted according
to the percentage of its variance that is explained by
August precipitation. The correlation between the esti-
mated and measured values gives the ‘‘effective correla-
tion’’ between August precipitation and the combination
of TRW and MVA. In our case, the ‘‘effective correla-
tion’’ between August precipitation and TRW combined
with MVA (r = 0.69) was higher than using TRW
(r = 0.49) and MVA (r = 0.61) alone.
The highest correlation coefficient (r = 0.76) occurred
between MAX and the precipitation in April–May (Fig. 6).
The significant negative correlation between October
temperature and MAX could result from a significant
negative correlation between May precipitation and Octo-
ber temperature (r = -0.51; P \ 0.05; n = 20).
The climate signal of 1/3MAX was better than MAX
and when we used two or three vessels was higher for 1/
3MVA[n] than for MVA[n] (Fig. 7). For the precipitation
in April–May, the signal of MVA[n] decreased with the
inclusion of more than one vessel, whereas for May–
June precipitation an increase of the signal was observed
when more than four vessels were considered. For the
first third of the ring, the addition of more vessels
reduced the climatic signal for April–May precipitation
and a negative trend in the correlation was observed for
14-16 >16
the better climatic signal was obtained using between 20
and 28 vessels from the first third of the ring
(1/3MVA[20BnB28]).
Trees (2010) 24:463–470 467

5 15
TRW MVA MAX
5 14
4
13

MAX (10 3 µm 2 )
MVA (10 3 µm 2 )
TRW (mm)

12
3
4
11

2
10
3
9
1
8

0 2 7

Growth index
Growth index
Growth index

1 1 1

1985 1990 1995 2000 2005 1985 1990 1995 2000 2005 1985 1990 1995 2000 2005
Year Year Year

Fig. 5 Raw and standard chronologies of tree-ring width (TRW), mean vessel area (MVA), and maximum vessel area (MAX). Each raw
chronology was smoothed with the use of a 32-year cubic spline (red line)

Table 1 Mean sensitivity (MS), mean correlation (Rbt), expressed

population signal (EPS) and first-order autocorrelation (AutoR) for
tree-ring width (TRW), mean vessel area (MVA) and maximum
vessel area (MAX) chronologies, for the common interval (1985–
2004)
TRW MVA
MS 0.30 0.13
Rbt 0.52 0.25
EPS 0.92 0.77
AutoR 0.25 0.09
Discussion
Tree rings, earlywood and latewood are easy to recognize
and measure, being the most common variables used for
dendrochronological research. The study of other anatom-
ical features, such as MVA and MAX, is more time-con-
suming and only worthwhile if they supply different
environmental information from that obtained with TRW
(Fonti and Garcı́a-González 2004; Fonti et al. 2009a).
According to our results, TRW of Q. ilex showed a stronger
common signal (EPS and Rbt) and a higher MS than vessel
features (MVA and MAX), suggesting that TRW is
apparently more appropriate for dendrochronological
studies. This was also observed by Fonti and Garcı́a-
González (2004) for C. sativa and by Corcuera et al. (2004)
for Q. ilex. Nonetheless, the common signal indicates the
statistical quality of each variable, but it does not describe
the climatic information recorded (Fonti and Garcı́a-Gon-
zález 2004). Thus, it is useful to compare the TRW and
vessel chronologies with climatic data.
Growth–climate correlations showed that TRW was
mainly correlated with the environmental conditions during
two periods, in spring and late summer, as expected under a
Mediterranean climate (Cherubini et al. 2003; Campelo
et al. 2007a). Precipitation during August (summer) also
MAX promoted an increase of TRW and this could be related to
the formation of new leaves in Q. ilex during wet summers
0.11
with the deposition of an extra growth band of xylem
0.20
(Corcuera et al. 2004; Campelo et al. 2007a). Other studies
0.71
also reported a positive influence of autumn precipitation in
0.24
the previous year on TRW of Q. ilex in France (Zhang and
Romane 1991; Cartan-Son et al. 1992), Portugal (Nabais
et al. 1998–1999; Campelo et al. 2009), Italy (Cherubini
et al. 2003) and Spain (Corcuera et al. 2004). In our study,
the lack of response of TRW to autumn precipitation of the
previous year reflects the low water-retention capacity of
the soil and the high dependence of wood cell development
on the current availability of photoassimilates.
The wood of Q. ilex can be classified as ‘‘diffuse to
semi-ring-porous’’, with wider vessels at the beginning and
gradually decreasing to the end of the ring (Carlquist 1988;
Woodcock 1994). Therefore, the largest vessels in Q. ilex
are formed during the early growing season and can be a
better proxy of the climate conditions during that period,
compared to TRW. Abundant water supply during the early
growing season enhances the formation of large vessels by
a high turgor pressure and rapid cell expansion (Tyree and
Sperry 1989; Sass and Eckstein 1995; Schume et al. 2004).
In fact, MAX was mainly correlated with precipitation in
April and May. Similar results were also found by Garcı́a-
González and Eckstein (2003) for the large earlywood
vessels of Q. robur. Precipitation in April enhanced MAX

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468 Trees (2010) 24:463–470

Tem perature P re c i p i ta t i o n
0. 8 0. 8
p <0 . 0 0 1
0. 6 0. 6
p <0 . 0 1
p <0 . 0 5
0. 4 0. 4

Correlation coefficient
Correlation coefficient

0. 2 0. 2
MV A
0. 0 MA X 0. 0
TRW
-0.2 -0.2

-0.4 -0.4
p <0 . 0 5
p <0 . 0 1 -0.6
-0.6
p <0 . 0 0 1

-0.8 -0.8
A S O N D J F M A M J J A S O N MA A M MJ A S O N D J F M A M J J A S O N MA A M MJ

Month Group of months Month Group of months

Fig. 6 Pearson’s correlation coefficients between the standard chro- last three bars on the right of each climatic variable represent groups
nologies of tree-ring width (TRW), mean vessel area (MVA), and of months (MA March–April, AM April–May, MJ May–June).
maximum vessel area (MAX) and monthly climatic data (mean air Horizontal lines indicate the significance levels for P \ 0.001,
temperature and total precipitation), for the period of 1985–2004. The P \ 0.01, and P \ 0.05 (n = 20)

April - May May May - June

0.8

P < 0.0001
Correlation coefficient

0.7
P < 0.001

0.6

P < 0.01
MVA[n]
MVA[n]
0.5
5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30
The n largest vessels

Fig. 7 Variation in Pearson’s correlation between mean vessel area (MVA[n]) and for the first third (1/3MVA[n]). Horizontal lines indicate
and precipitation in April–May, May and May–June as the number of the significance levels for P \ 0.0001, P \ 0.001, and P \ 0.01,
the largest vessels is progressively increased for the whole ring respectively

but had no effect on TRW, suggesting that the climatic and the prevailing climatic conditions during the growing
signal of MAX differs from TRW. Moreover, only MAX season. The only significant correlation found between
yielded an r C 0.71 for April–May and May–June precip- climate and MVA was with August precipitation from the
itation, meaning that precipitation in these periods explains previous year. Furthermore, the use of MVA associated
more than half of the variance in MAX. These findings with TRW enhanced our capacity to predict precipitation in
suggest that, in semiarid environments, MAX is a better August.
proxy for spring precipitation than TRW. The number of cambial cells differentiating into ves-
In evergreen Mediterranean species, the occurrence of sels is more or less constant during the whole growing
frequent small vessels throughout the whole ring represents season, as confirmed by the almost constant vessel
an appropriate strategy to cope with unfavourable condi- density throughout the whole ring (data not shown),
tions (freeze events in winter and drought periods in while the lumen area of vessels is mainly controlled by
summer), because small vessels are less susceptible to water availability throughout the growing season (Sass
cavitation and embolism (Sperry et al. 1994; Davis et al. and Eckstein 1995). According to Garcı́a-González and
1999). The occurrence of small vessels throughout the ring Fonti (2006), pooling vessels with different ontogeny
and the inclusion of vessels formed at different times can obscures the climatic signal, suggesting that only vessels
explain the lack of significant correlations between MVA formed within the same period should be used to explore

123
Trees (2010) 24:463–470
environmental signals. A good selection of vessels is
thus essential to maximize the climate signal and the
criterion could be the relative radial position within rings
and/or the vessel size. For April–May and May precip-
itation, the better climatic signal was attained by MAX
and was higher than when more vessels were included.
On the contrary, the use of more vessels improved the
climatic signal for May–June precipitation specially
when considering only the vessels present in the first
third of the ring (1/3MVA[n]). These results highlight the
effect of vessel ontogeny on the climatic signals
embodied.
The present study confirms the utility of vessel chro-
nologies as a record of intra-annual environmental condi-
tions in semiarid environments (Giantomasi et al. 2009).
Different environmental signals can be obtained if vessels
are selected according to their relative radial position
within the ring and then filtered by size. Based on our
results, vessel features from the initial part of the ring (1/
3MAX and 1/3MVA[n]) are promising climate proxies in
diffuse to semi-ring-porous species, as earlywood vessels
were previously used in ring-porous species (Garcı́a-Gon-
zález and Fonti 2006; Fonti et al. 2007; Fonti and Garcı́a-
González 2008). The largest vessels in Q. ilex provided a
distinct and stronger signal for the early season than TRW.
Vessel features, combined with other variables (e.g. TRW),
are expected to improve intra-annual climatic signals,
increasing the resolution of the climate reconstructions for
the Mediterranean region.
Acknowledgments Filipe Campelo was supported by Fundação
para a Ciência e Tecnologia (FCT), Portuguese Ministry for Science
and Technology, through a PhD fellowship (SFRH/BD/10677/2002)
and by the EC project Millenium (Grant no. 017008). We thank two
anonymous reviewers for their comments on an earlier draft of this
article.
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