ORIGINAL ARTICLE
Long-term effect of temperature and precipitation on radial
growth in a threatened thermo-Mediterranean tree population
Magdalena
_
Zywiec
1,5
•
El
_
zbieta Muter
2
•
Tomasz Zielonka
3
•
Miguel Delibes
4
•
Gemma Calvo
4
•
Jose M. Fedriani
4,5
Received: 20 June 2016 / Accepted: 27 September 2016 / Published online: 11 October 2016
Ó The Author(s) 2016. This article is published with open access at Springerlink.com
Abstract
Key message Based on the first dendroclimatological
analyses of the thermo-Mediterranean tree Pyrus
bourgaeana, the positive relationship between the
growth and climate (i.e., precipitation) has strengthened
in recent decades.
Abstract The combined effect of climate change and
habitat destruction and fragmentation threatens many plant
populations and even entire communities in Mediterranean
ecosystems. The Iberian pear, Pyrus bourgaeana Decne, a
characteristic species of Mediterranean ecosystems, is
threatened by both habitat and climate changes. We ask
whether and how the growth of mature P. bourgaeana in
the thermo-Mediterranean zone (i.e., altitude \700 m) has
been affected by long-term climate changes during the last
century in a fragmented land scape. Dendrochronological
methods were used to find growth–climate relationships.
We made the first dendroclimatological analyses and con-
structed a first 103-year tree-ring chronology (1905–2007)
of this species . The tree-ring series revealed large growth
variability. We found a clear, strong relationship between
tree growth and climate, with annual precipitation being
the most important climate factor enhancing radial growth.
Our results also showed that warm autumns and winters
positively affect growth. There was no temporal stability in
the relationship between tree growth and climate. The most
general trend was in the relationship between annual pre-
cipitation and tree growth: the decrease of rainfall in the
last decades of the twentieth century was associated with a
constant increase of the correlation coefficient. Water
accumulated in the soil in autumn and winter proved to be
a key factor augmenting tree growth in the following
vegetation period. The climate–growth relationship in P.
bourgaeana has strengthened in recent decades apparently
due to decreased precipitation levels.
Keywords Climate change Dendrochronology Iberian
pear Pyrus bourgaeana Thermo-Mediterranean zone
Tree growth
Introduction
Most models of climate change predict global warming
associated with a marked variation of the level and spatio-
temporal distribution of precipitation and temperature
(IPCC
2014; Fischer and Scha
¨
r 2010; Hoerling et al. 2012).
Ecosystems of all climate zones are vulnerable to climate
change, even in environments where water is not consid-
ered a limited resource (Allen et al.
2010), but according to
climate models, the Mediterranean Basin is one of the
Communicated by E. Liang.
& Magdalena
_
Zywiec
m.zywiec@botany.pl
1
Władysław Szafer Institute of Botany, Polish Academy of
Sciences, ul. Lubicz 46, 31-512 Krako
´
w, Poland
2
Department of Forest Biodiversity, Institute of Forest
Ecology and Silviculture, Faculty of Forestry, University of
Agriculture in Krakow, Al. 29 Listopada 46, 31-425 Krako
´
w,
Poland
3
Institute of Biology, Pedagogical University of Cracow, ul.
Podchora˛
_
zych 2, 30-084 Krako
´
w, Poland
4
Department of Conservation Biology, Estacion Biologica de
Don
˜
ana (EBD–CSIC), c/Americo Vespucio s/n,
41092 Seville, Spain
5
Centre for Applied Ecology ‘‘Prof Baeta Neves’’(CEABN-
InBIO), School of Agronomy, University of Lisbon, Tapada
da Ajuda, 1349-017 Lisbon, Portugal
123
Trees (2017) 31:491–501
DOI 10.1007/s00468-016-1472-8
world’s climate change hotspots because of increases in the
frequency, duration, and/or severity of droughts and heat
stress (IPCC
2014; Luterbacher et al. 2012; Anderegg et al.
2013; Barbeta et al. 2013). Moreover, land-use change and
habitat fragmentation are also important factors rapidl y
altering the composition of communities in Mediterranean
ecosystems (Linares et al.
2010; Olano et al. 2012; Mate-
sanz et al.
2015). Therefore, a full understanding of the
level of tolerance to climate change is particularly needed
in such human ized Mediterranean habitats to forecast
population trends and distribution of threatened tree
species.
Changes in temperature and water availability often
have marked effects on tree growth (Schweingruber
1996).
Because trees are long-lived organisms, their ring series
record long-term year-to-year changes in climate condi-
tions (Schweingruber
1996; Nicault et al. 2008 ; Olano et al.
2008, 2012). Due to their complex physiology, trees may
respond to climatic changes in complex ways (Drew et al.
2013; Olano et al. 2014; Zang et al. 2014). Moreover,
changes in the constraining factors may cause temporal
instability in the relationship between climate and tree
growth that modulates the response patterns of tree growth
(Briffa et al.
1998, 2002; D’Arrigo et al. 2008; Briffa and
Matthews
2002; Leburgeois et al. 2012).
In the thermo-M editerranean zone (i.e., altitude below
700 m; Olson et al.
2001) climate imposes a double
adversity for growth and survival of shrubs and trees, i.e.,
extreme summer droughts and erratic, unpredictable rain
(Valladares et al.
2014). Global climate change is generally
resulting in higher temperatures and lower precipitation,
though such changes are not distributed uniformly
throughout the year. As a consequence, the effect of cli-
mate change on tree-ring formation can vary depending on
the relative importance of the two main limiting climate
factors, making predictions particularly difficult. At higher
altitudes, e.g., meso-, supra-, and oro-Mediterrranean zones
(700–2700 m; Olson et al.
2001), where winter cold can be
an important stressor, no agreed-upon trend in the response
of tree growth to climate change has been inferred from
long tree-ring series (Granda et al.
2013, 2014). Some
studies have documented an increase (Martinez-Vilalta
et al.
2008; Vila et al. 2008; Gimeno et al. 2012; Tegel
et al.
2014), and others, a decrease in the growth of
Mediterranean trees during the second half of the twentieth
century (Jump et al.
2006; Saris et al. 2007; Piovesan et al.
2008; Di Filippo et al. 2010
). Changes in climate–growth
relationships have also been reported for several Mediter-
ranean tree species (Andreu et al.
2007; Planells et al.
2009; Carrer et al. 2010; Leburgeois et al. 2012). However,
the existing data are based mostly on widespread evergreen
trees (e.g. Viera et al.
2009; Campelo et al. 2010; Martin-
Benito et al. 2011, 2013; Candel-Perez et al. 2012; Gimeno
et al.
2012), and deciduous species have been much less
studied in the Mediterranean area (e.g., Tegel et al.
2014;
Gonza
´
lez-Gonza
´
lez et al.
2015). Even less is known about
the response to climate change of small trees and shrubs at
low altitudes in the thermo-Mediterranean.
In this study, we examined long-term changes in the sta-
bility of the climate–growth relationship of a thermo-
Mediterranean deciduous small tree, to gain a perspective on
the future persistence of this species, which has been deci-
mated by different components of global change. Our model
plant, the Iberian pear (Pyrus bourgaeana Decne), is a
characteristic species of Medi terranean ecosystems and is
considered important to their functioning (Cabezudo and
Pe
´
rez Latorre
2004; Fedriani et al. 2010; Arenas-Castro et al.
2013). In Don
˜
ana National Park (SW Spain), P. bourgaeana
trees often occur at low density in small scrubland patches
among farmland, towns, and other built-over areas (Fedriani
et al.
2010). Currently, P. bourgaeana shows a very low level
of natural regeneration, most likely because of dispersal
limitation, extreme summer droughts, and increased herbi-
vore pressure, limiting seedling establishment (Fedriani et al.
2010, 2015). It is unclear whether and how mature P. bour-
gaeana tree growth has been affected by long-term changes
in climate thr ough the last century. This should be a funda-
mental step to predict the fate of the species, and, in general,
of other deciduous thermo- and meso-Mediterranean shrubs
and small trees, under a scenario of global warming.
Specifically, in this study, we sought to answer the following
two questions: (1) what sort of long-term climate–growth
relationship is shown by P. bourgaeana?, and (2) is this
relationship temporally stable, and if not, what is the trend of
such/these changes, (if found any)?
Methods
Study site
The study site is located in southwestern Spain, in the
Don
˜
ana World Biosphere Reserve (37°9
0
N, 6°26
0
W;
0–80 m a.s.l.) on the west bank of the Guadalquivir River
estuary. The Don
˜
ana area comprises three main ecosys-
tems: mobile dunes, scrubland (where P. bourgaeana
grows), and marshes. In the tree layer, in addition to our
focal species, there are scattered Quercus suber, Olea
europaea var. sylvestris, Fraxinus angustifolia, and Pinus
pinea. In the understory, there are Pistacia lentiscus,
Halimium halimifolium, Ulex spp., Chamaerops humilis,
and Erica sp. (Valverde
1958; Fedriani et al. 1998, 2010).
P. bourgaeana trees occur at low densities (generally less
than one individual per ha; Fedriani et al.
2010) in patches
of Mediterranean scrubland that are isolated from each
other by natural or anthropogenic barriers (marshes, sand
492 Trees (2017) 31:491–501
123
dunes or cultivations) (see also
_
Zywiec et al. 2012 for
details).
Climate data
Climate data were obtained from the Spanish Agencia
Estatal de Metereologı
´
a (AEMET) meteorological station
located in Sevilla, the closest (ca. 80 km away) meteoro-
logical station providing long-term data and located near
sea level (11 m a.s.l). Continuous data for daily mean
temperature and daily total precipitation were available
since 1946. We calculated mean temperature and accu-
mulated precipitation for each month, as well as annual
accumulated precipitation. Annual accumulated precipita-
tion was summed from the September of the previous year
to the August of the current year.
The climate is Mediterranean sub-humid, and is charac-
terized by dry, hot, long summers (June–September) and
mild, wet winters (November–February). In the stud y period
(from 1946 to 2007), mean annual temper ature varied con-
siderably (Fig.
1a). The highest temperatures were recorded
at the beginning and at the end of our studied period. The
lowest temperatures occurred in the early 1970s and then
increased consistently until the first decade of the twenty-
first century. Total annual precipitation also varied mark-
edly, but no conspicuous temporal trend was found (Fig.
1a;
R
2
= 0.003, F
1,59
= 1.20, P = 0.28). Groundwater avail-
ability shows marked seasonal changes in this area (Instituto
Tecnologico Geominer o Espan
˜
ol,
1992). Precipitation is
highest in the winter and lowest in the summer. The distri-
bution of precipitation in a year changed along a studied
period. The precipitation of January, February and March
decreased considerably and the precipitation of October,
November and December increased in the second half of the
period considered in the study (Fig.
1b).
Study species
Pyrus bourgaeana Decne (Rosaceae) is a broadleaved
deciduous tree. It is native to the Iberian Peninsula (Spain,
Portugal) and North Africa (Morocco) (Aldasoro et al.
1996). It typically reaches 3–6 m height. Budburst occurs
from February to April, and leaf senescence from June to
September (Mediavilla and Escudero
2003; Arenas-Castro
2012). It flowers during February–March, is hermaph rodite
and self-incompatible (
_
Zywiec et al.
2012; Authors, un-
published data). In Don
˜
ana, annually, each P. bourgaeana
tree typically produces between 200 and 450 fleshy fruits
which ripen during the autumn (September–November;
Fedriani et al.
2015). The fruits are non-dehiscent globose
pomes (2–3 cm diameter) weighing ca. 6.7 g, with sugary,
juicy pulp (Fedriani et al.
2012).
Fig. 1 a Mean annual
temperature (1946–2007) and
total annual precipitation
(1946–2007) near the study
area; data from Sevilla weather
station and b Climate diagrams
for the meteorological station in
Sevilla (37°23
0
10
00
N,
5°59
0
33
00
W, 11 m a. s. l.) for the
periods 1946–1976 and
1977–2007 indicating the intra-
annual distribution of monthly
mean temperatures (line) and
monthly total precipitation
(bars); MAT mean annual
temperature (°C) and MAP
mean annual precipitation [mm]
Trees (2017) 31:491–501 493
123
The Don
˜
ana population of P. bourgaeana has limited
reproduction and regeneration ability (Fedriani and Delibes
2009; Fedriani et al. 2010, 2012). Our unpublished data
indicate that the Don
˜
ana population of this long-lived tree
shows a marked left-skewed demographic str ucture, with
many individuals in older age classes, few juveniles, and
even fewer seedlings and saplings. Despite the sparseness
of this population, P. bourgaeana fruit, seeds, seedlings,
and leaves represent important resources for diverse animal
guilds, especially during the dry summers (e.g., Fedri ani
and Delibes
2009; Fedriani et al. 2012); so, its pers istence
is critical to the ecologi cal stability of the community.
Data collection
Trees (n = 32) were sampled in winter and spring of 2008
and 2009. Tree clusters grow scattered in Mediterranean
scrubland, in similar light conditions representing the
uppermost vegetation layer. Their mean diameter (dbh)
was 18 cm (±11). The trees were cored with an increment
borer (diameter 5 mm) ca. 40 cm above the tree base. The
cores were glued to wood slats, dried and polished with a
belt sander (progressively up to grid 600) to make the tree-
ring sequences clearly visible. The samples were scanned
at 2400 dpi resolution. W
INDENDRO (
http://www.regentin
struments.com/assets/windendro_about.html
) was used to
measure the annual tree-ring widths to 0.01 mm accuracy .
Core sections with extremely narrow, missing or false rings
were carefully checked under a stereomicroscope at
7–459. The quality of dating was checked with the C
OFE-
CHA program (Dendrochronology Program Library, Holmes
and Cook
1983). All measurement series with potential
errors were re-checked once again and corrected if dating
errors were found (Holmes et al.
1986).
Data analysis
Tree-ring chronology
We calculated the index series to study the influence of
climate factors on tree growth (Holmes
1994). Individual
raw ring-width series were standardized using ARSTAN
software by fitting a horizontal line through the mean
values of the series , and, in the next step, by dividing the
measurement in every year by the mean value calculated
for each series (Holmes
1994). Then, we performed
autoregressive modeling of the index series to remove
autocorrelations and enhance the common signal of the
trees. After that, the indices of individual trees were
averaged to an indexed chronology by applying a biweight
robust mean (Holmes
1994). The first-order autocorrelation
of the 1904–2007 raw chronology (a measure of the lagged
effect of ring width from the previous year on next-season
growth) was 0.455, and the first-order autocorrelation of
the indexed chronology was -0.137. This means that a
great part of the autocorrelation was removed in the pro-
cess of constructing the indexed chronology allowing
dendroclimatological analyses.
Mean sensitivity, expressing the interannual variability
of ring width, was calculated for the indexed chronology
1947–2007 (Fritts
1976). For the period 1947–2007, we
also calculated the expressed population signal (EPS),
which quantifies how well a chronology based on a finite
number of trees represents the hypothetical perfect or true
chronology (Wigley et al.
1984).
Weather factors influencing tree growth and temporal
changes in the climate–growth relationship
The indexed chronology was used for calculation of the
tree growth–climate relationship. To evaluate the potential
relationship between tree growth and annual precipitation,
we performed several simpl e regression analyses, first
regressing the indexed chronology and year, and then,
annual precipitation and year. Then, we used the residuals
from those two previous analyses and regressed them to
evaluate their potential relationship once the effect of year
was corrected for (e.g., Ovaskainen et al.
2013).
The relationships between tree growth and monthly
climatic conditions (mean monthly temperature, total
monthly precipitation) were calculated through correlation
and response function analyses with DendroClim2002
(Biondi and Waikul
2004). The program applies a boot-
strap process to assess the statistical significance of the
correlations.
Time-dependent changes in the relationship between
tree growth and climate factors were analyzed using Den-
droClim2002 as well. The correlations of indexed
chronology with total monthly precipitation and mean
monthly temperature (from previous September to current
June) were done for 30-year periods. The moving corre-
lation windows (32 periods) were progressively shifted by
1 year over time at each iteration (the first for 1947–1976
and the last for 1978–2007). Moreover, for each 30-year
period, climatic conditions were defined as mean monthly
precipitation and mean monthly temperature.
Results
Patterns of tree growth
The constructed indexed chronology (based on 32 P.
bourgaeana trees) covers a 103-year time span
(1905–2007; Fig.
2a, b). The two oldest trees had 104 rings
(at ca. 40 cm height). Mean ring width was 1.34 mm
494 Trees (2017) 31:491–501
123
(±1.04) for 1947–2007, and 1.35 mm (±1.04) for
1904–2007; it reached maximum of 7.83 mm in 1996 as
calculated from the raw chronology. The mean sensitivity
of the indexed chronology for 1947–2007 was 0.49. The
expressed population signal (EPS) for 1947–2007 was
0.87. With time, the number of years for which the tree
series showed no ring formation (missing ring) increased:
in the 1950s and 1960s, there were no absent rings; in the
1970s, 1 year had no ring (1974; 2 trees); in the 1980s,
there were 4 such years (1980, 1981, 1983, 1989; 1 tree
each year); in the 1990s, there were 5 such years
(1992–1995 and 1999;1–3 trees each year); and in the first
7 years of the twenty-first century, there was 1 year with a
missing ring (2005; 1 tree).
Long-term climate–growth relationship
Tree growth was strongly and positively related to annual
precipitation, summed from September of the previous year
to August of the current year (Fig.
2b; regression of
residuals: R
2
= 0.66, F
1,59
= 114.25, P \ 10
-4
). Tree
growth was not correlated with total precipitation of the
preceding year (regression of residuals: R
2
= 0.01,
F
1,58
= 0.28, P = 0.60). Correlation coefficients showed
that precipitation from November of the previous year to
January of the current year was especially important for
tree growth (Fig.
3). Almost the same was found using
response function coefficients; precipitation of previous
October, previous November, and January and February of
the current year positively affected growth (Fig.
3). Pre-
cipitation from February to June of the current year also
positively influenced growth, with June precipitation being
the most important among those months (Fig.
3).
Mean monthly temperature influenced tree growth less
than precipitation did (Fig.
3). There was a positive cor-
relation between tree growth and temperature of the pre-
vious October. High winter temperature (previous
December and current January) also influenced growth
positively, but this relationship was significant only for
current January temperature. High temperature from April
Fig. 2 Row chronology of P.
bourgaeana in the Don
˜
ana area
with number of measured trees
(a) and indexed chronology
with annual precipitation
records from the Sevilla weather
station (b)
Trees (2017) 31:491–501 495
123