Tree Physiology 20, 893–900
© 2000 Heron Publishing—Victoria, Canada
Influence of weather on cork-ring width
ANTONIA CARITAT,1 EMILIA GUTIÉRREZ2 and MARISA MOLINAS1,3
1
Laboratori del Suro, University of Girona, Campus Montilivi, E-17071 Girona, Spain
2
Department of Ecology, University of Barcelona, Avinguda Diagonal 645, E-08028 Barcelona, Spain
3
Author to whom correspondence should be addressed
Received August 4, 1999
Summary Ring-width series of cork from Quercus suber L.
trees growing at two sites in Extremadura (southwestern
Spain) were analyzed in relation to monthly precipitation and
temperature, and to climatic indices combining both variables.
Ring width of cork showed strong positive correlations with
precipitation, especially during the fall and winter. Moderately
low temperatures were favorable for cork growth, except in
winter and during the onset of phellogen activity. We conclude
that drought or temperature, or both, can limit cork growth during the annual drought period.
Keywords: climatic variability, cork growth, cork-ring chronology, dendroclimatology, phellogen activity, Quercus suber.
Introduction
Quercus suber L., which is well known for its cork production,
is an evergreen oak that grows on siliceous substrates and is
widely distributed in the western Mediterranean region. The
xerophytic character of the cork tree is seen in features such as
sclerophylly, the presence of a lignotuber (Molinas and Verdaguer 1993a, 1993b), litterfall pattern (Caritat et al. 1996a),
and stomatal response to water deficit (Tenhunen et al. 1984,
Oliveira et al. 1992). In Q. suber, the cork cambium (phellogen) is a permanent layer that adds a new layer of cork to the
outer bark (phellem) of the tree each year. The phellogen usually becomes active in April and may remain active until the
end of October (Natividade 1950). Cork ring boundaries are
clearly demarcated because spring cells have thinner walls and
larger diameters than those formed later in the season. Cork
from wild trees is deeply furrowed and irregular, making it difficult to identify the rings. However, the natural or wild cork
must first be removed to obtain commercial cork, and the new
growth is much more uniform and forms more regular rings.
Wild cork is removed when the tree is about 30 cm in diameter
(about 30–40 years old). Henceforth, commercial cork is removed each time the bark reaches at least 25 mm in thickness,
resulting in harvest intervals (referred to as cork peel-off turns)
of 8–14 years, depending on the area. The cork is harvested
only during the season when the tree is in sap and the layers
separate more easily, usually beginning in June and lasting until August. For a more regular distribution of the cork harvest,
an alternate system is followed in which only some trees are
stripped each season.
Because most phellems do not show annual growth rings,
little is known about interannual variability in phellem growth
or about how climatic factors affect phellogen activity (Waisel
1995). Nevertheless, cork rings of Q. suber can be dated and
subjected to climatic analysis. A previous study by Caritat et
al. (1996b) established a 14-year cork-ring chronology and reported evidence of the influence of precipitation and temperature on ring width variability of cork. The present study
extends this previous chronology and constructs a new one
from a different site in the same area. Both chronologies were
analyzed in relation to precipitation, temperature and combined climatic indices. The objectives were: (1) to determine
the influence of climate on the interannual pattern of ringwidth variability of cork, and (2) to analyze the relationship
between cork growth and climatic variables. The overall objective was to assess to what extent summer drought affects
cork growth in an area characterized by Mediterranean climatic conditions.
Materials and methods
Study area
The two study sites, La Herguijuela (Campo Arañuelo,
Cáceres) and Torre Sirgada (Jerez de los Caballeros, Badajoz),
were chosen for their different topographic conditions in
Extremadura (southwestern Spain) (Table 1). At both sites, the
cork woodland is a multipurpose forest or dehesa used for
livestock and cork production. At La Herguijuela, the cork
trees are partially stripped each year, whereas at Torre Sirgada
cork-stripping campaigns take place every 2 years. At both
sites, cork harvests occur at 10-year intervals.
Samples and data collection
Cork samples of 10 × 10 cm 2 were taken at breast height and in
the same southern orientation during the stripping of the trees.
To observe the growth rings, the samples were boiled in water
for about 45 min to prepare them for thin sectioning (Figure 1).
Total bark thickness was measured, rings were counted and
dated, and a visual synchronization was carried out. The wid-
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CARITAT, GUTIÉRREZ AND MOLINAS
Table 1. Topographical and forestry parameters of the La Herguijuela and Torre Sirgada sites in Extremadura (southwestern Spain).
Parameter
La Herguijuela
Torre Sirgada
Geographic coordinates
Altitude (m a.s.l.)
Annual precipitation (mm)1
Soil parent material
Slope (%)
Tree age (range, years)
Tree density (ha –1)2
Tree height (mean ± SD, m)2
DBH (mean ± SD, cm)2
Bifurcation height (mean ± SD, m)2
Cork ring width (range, mm)
Cork ring width (mean ± SD, mm)
Shrub stratum
05°55′ W, 39°6′ N
300–400
777.5
Alluvial debris
5–7
150–170
30
6.89 ± 0.95; n = 15
62 ± 4; n = 15
2.47 ± 0.20; n = 15
1.85–5.25
3.30 ± 0.96
No shrub stratum present
Herbaceous stratum
Annual grasses with Tuberarietalia guttatae
(L.) Fourr. being the most abundant species.
06°50′ W, 38°23′ N
500–600
606.2
Shale
20
25–160
57
8.91 ± 2.20; n = 18
69 ± 15; n = 18
3.24 ± 1.25; n = 18
1.95–4.70
3.56 ± 0.95
Low shrub stratum with Cistus salvifolius L. and C. crispus L.
Annual grasses with Aegylops geniculata, Plantago sp. and Briza maxima L.
equally abundant.
1
2
Annual precipitation for the period 1979–1995.
Values for mature trees under cork extraction.
est and narrowest rings were used as markers. The initial and
final rings were rejected as being associated with incomplete
growth periods. For each cork sample, cork-ring series were
identified along three radii. Ring widths of the cork were measured with a 10× binocular microscope equipped with a micrometer scale.
Climatic data were obtained from nearby weather stations
belonging to the Centro Metereológico Territorial de Extremadura (Spain). Precipitation and temperature series from the
Malpartida weather station (23 km from the La Herguijuela
site) and from Jerez de los Caballeros station (10 km from the
Torre Sirgada site) were used (Figure 2). To assure the quality
Figure 1. Cork specimen from La Herguijuela, Cáceres, Spain. Note
the presence of cork rings of different width.
of the records, climatic series from Malpartida were checked
against Salto de Torrejón (220 m a.s.l., 0.5 km from La Herguijuela); the series from Jerez de los Caballeros were checked
against Valencia de Mombuey (297 m a.s.l.) and Fregenal de
la Sierra (580 m a.s.l.), located 25 and 16 km from Tore
Figure 2. Climate diagrams for the study period (1979–1995) for
Malpartida (Campo Arañuelo, Cáceres) and Jerez de los Caballeros
(Badajoz). Symbols: 䊊, temperature; 䊉, precipitation. Note the
occurrence of the drought season in summer and to a lesser extent in
spring. Note the marked drop in precipitation at the beginning of the
summer drought season in La Herguijuela. Temperature and precipitation values at the top of the graphs are mean values.
TREE PHYSIOLOGY VOLUME 20, 2000
SENSITIVITY OF CORK GROWTH TO CLIMATE
Sirgada, respectively. Pearson correlation coefficients (r) between the monthly climatic variables of Malpartida and Jerez
were significant for precipitation (r = 0.84, P < 0.001, n = 17)
and temperature (r = 0.63, P < 0.01, n = 17).
Cork-ring series and data analysis
To establish the mean ring width chronology of the cork for
each site, we obtained mean harvest-year series and then overlapped and averaged the successive harvest-year series. To obtain a mean harvest-year series, a cork growth curve was built
for each sampled tree and the individual series were compared
with each other using multiplot representations for visual corroboration (Cook and Kairiukstis 1990). The Pearson correlation coefficient (r) between the series was calculated to verify
synchronization and the series showing statistically significant coefficients were averaged. For La Herguijuela, six harvest-year series (1989, 91, 93, 94, 95 and 96) were overlapped.
The 93 series was formed from 46 out of 57 individual-tree series (Caritat el al. 1996b). The 89, 91, 94, 95 and 96 series were
formed from 13 out of 15, 11 out of 13, 5 out of 10, 9 out of 12,
and 10 out of 13 individual series, respectively. For Torre Sirgada, three harvest-year series (1989, 92 and 95) were overlapped. At this site, the 89 and 92 series were formed from four
out of 10 individual series and the 95 series was formed from
eight out of 12 individual series. A series was selected if its coefficient of correlation (Pearson’s r) was significant at P <
0.05.
Cork-ring chronologies showed a decreasing trend in ring
width with time that was attributed to aging (Natividade
1950). To minimize this effect and maximize the interannual
fluctuations due to climate, each series of raw data was standardized by means of the empirical growth function: Yt =
atbe –ctEt, where Yt = ÿt E t, where Yt is the actual measurement of
ring width (RW), ÿt is the estimated value, and E t is the residual or remainder, called growth index (GI) in dendrochronological studies (a, b and c = constants; t = time) (Warren
1980). The standardized series of growth indices were assumed to be constant with respect to the mean and variance.
Effect of climate on cork rings
The influence of climatic factors on the interannual pattern of
ring width was measured by means of the Pearson correlation
coefficient (r). The relationship between cork growth and climatic factors was analyzed by means of paired analyses and
bivariate scatterplots in which ring width (RW) or growth index (GI) was used as the dependent variable. The mathematical functions showing the best fit were then selected. The
Bonferroni method (Sokal and Rohlf 1995) was used to limit
the overall experimental error rate. The climatic variables considered were monthly precipitation (mm), precipitation accumulated during selected periods, mean monthly temperature
(Tm), mean maximum temperature (Tx-M), the mean minimum
temperature (Ti-M), absolute maximum temperature (Tmax), and
absolute minimum temperature (Tmin). We also considered the
drought index formed by the quotient between annual precipitation and mean annual temperature (P/T + 10) and several
895
other indices designed to unmask the effects of water deficits
on cork growth. These indices were formed by using precipitation in periods with high positive effect (see Table 2) divided
by temperatures with high negative effect (spring or summer
months) or divided by combinations made by subtracting temperatures with positive effect (usually April or May) from
temperatures with high negative effect. Multiple linear regression analysis was also used to assess the relative predictive capabilities of climatic independent variables.
Results
Chronologies
At both sites, the individual tree series in each harvest year
were closely correlated with one another (La Herguijuela
mean r ± SD = 0.81 ± 0.08, P < 0.05; Torre Sirgada = 0.74 ±
0.09, P < 0.05). The correlation coefficients between sites for
the overlapping years were r = 0.703 (n = 13 years in common,
P < 0.01) for growth indices and r = 0.678 (n = 13, P < 0.02)
for ring width.
The range of ring widths (Table 1) was typical of mature
cork trees (100–150 years old) in the dehesa of southwestern
Spain (Caritat et al. 1996b), and comparable with wood-ring
chronologies established in other regions of Spain (PérezAntelo 1994, Gutiérrez et al. 1998). Generally, the years of
maximum and minimum cork growth were common to both
sites (r = 0.678, P < 0.02) (Figure 3). Interannual variability in
cork growth indices, as measured by the mean sensitivity coefficient MSx (Fritts 1976), was high. The MSx was 0.185 (RW)
and 0.167 (GI) for trees at La Herguijuela, and 0.222 (RW)
and 0.214 (GI) for trees at Torre Sirgada.
Response to precipitation
The effects of monthly precipitation on cork growth indices
are given in Figure 4. Most correlation coefficients were not
significant; however, precipitation in January had a significant
positive effect at both sites, and precipitation in June and July
had a positive effect that was significant at La Herguijuela.
Precipitation in October showed a negative correlation that
was significant at Torre Sirgada. However, because October
rainfall is thought to contribute to cork growth, we tested its
correlation with growth indices of the following year (t + 1)
and found a positive correlation at both sites that was significant at La Herguijuela. The responses to accumulated precipitation over certain months were more striking than the effect
of monthly precipitation, especially for trees at La Herguijuela. The highest correlations were obtained when rainfall
from autumn and winter months of the preceding year was
added to that of the spring and summer of the current year (Table 2). As shown in Figure 5, cork growth was synchronous
with accumulated precipitation. A shift in the mean amount of
precipitation occurred in 1989, and this shift was also observed in the cork series, most strikingly in the ring-width
chronologies.
The scatterplots pairing ring-width data with accumulated
precipitation showed a strong and positive relationship that
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CARITAT, GUTIÉRREZ AND MOLINAS
Table 2. Pearson correlation coefficients (r) between annual cork growth indices (GI) and ring width (RW) and the accumulated mean monthly
precipitation for certain periods. Asterisks indicate statistically significant coefficients (* = P < 0.05, ** = P < 0.01, and *** = P < 0.001). (The
Bonferroni adjusted α was 0.0045).
Period of precipitation
January to June
January to December
February to April
March to June
May to September
June to September
November (t – 1) to June
November (t – 1) to July
November (t – 1) to September
October (t – 1) to June
October (t – 1) to September
October (t – 1) to December (t – 1)
La Herguijuela (n = 17)
Torre Sirgada (n = 13)
RW
GI
RW
0.666*
0.437
0.163
0.464
0.572*
0.677**
0.705**
0.746***
0.781***
0.572*
0.668**
0.285
0.796***
0.351
0.150
0.481
0.668**
0.454
0.691**
0.725***
0.721**
0.712*
0.770***
0.384
0.088
0.011
0.149
–0.406
–0.244
–0.098
0.528
0.545
0.598*
0.314
0.395
0.320
was generally linear (Figures 6a, 6b and 6d). However, there
was a nonlinear relationship between ring width and accumulated precipitation from November (t – 1) to June (t) at Torre
Sirgada (Figure 6c), indicating that, after a threshold amount
of precipitation, the increase in ring width decreased with further increases in precipitation.
GI
0.345
–0.137
0.147
–0.237
–0.141
–0.123
0.538
0.544**
0.691**
0.684**
0.757**
0.566*
Figure 8 depicts selected examples of bivariate analysis of
temperature and cork growth indices. The relationship with
November Tmin showed a gradual decrease in cork growth as
temperature increased (Figure 8b). In the scatterplot that
Response to temperature
Temperature responses were built using the growth indices to
minimize the effect of precipitation. The correlation coefficients with monthly temperatures were low, being mostly negative and not statistically significant (Figure 4). There was a
high negative correlation for almost all March temperatures,
which was significant for Ti-M in trees at Torre Sirgada. The
negative effect of March temperatures on the cork growth indices might be attributed to the early spring dry period that
usually occurs in March in this area (Figure 2). The general inverse relationship between cork growth and temperature was
more pronounced in trees at Torre Sirgada than at La
Herguijuela (Figure 7). At Torre Sirgada, cork growth was
lowest in 1993 when March Ti-M was highest. At La Herguijuela, cork growth was highest when July Tm reached its
minimum value for the study period (1987 and 1988).
Figure 3. Cork growth indices from La Herguijuela and Torre Sirgada.
Figure 4. Response of cork growth indices to precipitation (P) and
temperature (T ) based on Pearson correlation coefficients (r) at La
Herguijuela (n = 17 years, 1979–95) and at Torre Sirgada (n = 13
years, 1982–94). Symbols: 䊊, Tm, monthly mean; ⵧ, Tmin, absolute
minimum; 䉭, Tmax, absolute maximum; 䉮, Ti-M, mean minimum; 䉫,
Tx-M, mean maximum temperatures. Asterisks indicate statistically
significant correlation coefficients (P < 0.05).
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SENSITIVITY OF CORK GROWTH TO CLIMATE
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even if precipitation was high. The nonlinear relationship with
March Ti-M at Torre Sirgada indicates that cork growth rate
was almost constant between 5 and 7 °C, but decreased at
higher temperatures (Figure 8c).
Joint effect of precipitation and temperature
Figure 5. Series of ring widths of cork (䊉) and growth indices (䊏) in
relation to accumulated precipitation (䊊) at La Herguijuela. (a) Precipitation from November (t – 1) to June (t), and (b) from January to
June.
paired cork growth indices and July Tm at La Herguijuela, an
exponential pattern emerged when the boundary points (circled dots) were selected (Figure 8a). There was a marked decrease in cork growth when the temperature was above 28 °C,
The correlation coefficients between cork growth and the
drought index, P/T + 10, were low and not significant. However, for the indices designed to emphasize soil water deficits,
the correlation coefficients for the drought index were usually
greater than those for precipitation or temperature considered
separately (Figure 9). In general, the relationship followed a
common pattern that fitted the function Y = ax b (Figures 9b–f).
However, in one case it was a linear relationship (Figure 9a),
indicating that, at La Herguijuela, cork growth was proportional to an increase in accumulated precipitation for the January to June period, or to a decrease in July Tmax. The most
common nonlinear behavior was caused by the limiting effect
of precipitation or temperature. If temperature was high compared with precipitation, a narrow ring was formed even if precipitation was abundant. Years with such behavior differed
between the two sites because of small local climatic differences.
The relationship between annual cork growth and the independent climatic variables, precipitation and mean temperature, exhibited adjusted R 2 values of 0.66 (La Herguijuela) and
0.64 (Torre Sirgada). The relationship was explained by the
equations: GR = 0.519 + 0.00152P1–9 for La Huerguijuela and
GR = –0.024 + 0.00109P11–9 + 0.035T3 for Torre Sirgada,
where GR is annual cork growth, P1–9 is precipitation from
Figure 6. Relationship between
cork ring width (RW) and precipitation. Scatterplots for the
periods (a) January to June and
(b) November (t – 1) to September (t) at La Herguijuela;
and (c) November (t – 1) to
June and (d) November to September at Torre Sirgada. The
goodness of fit, R 2, and the significance level, P, are given in
each figure.
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CARITAT, GUTIÉRREZ AND MOLINAS
Figure 7. Series of ring widths of cork (䊉) and growth indices (䊏) in
relation to temperature (䊊). (a) Monthly mean July temperature (Tm)
for La Herguijuela, and (b) March mean minimum temperature (Ti-M)
for Torre Sirgada.
January to September, P11–9 is precipitation from November of
the previous year to September and T3 is the mean temperature
in March.
Discussion
Cork cambium dynamics are sensitive to climatic factors.
Cork-ring growth was high in rainy years (Figure 5) and during years in which temperature was moderately low (Figure 7).
The decrease in precipitation recorded after 1989 at La Herguijuela and the increase in March Ti-M recorded after 1984 at
Torre Sirgada could explain the trend of decreasing cork
growth with time at both sites. The ring-width series were
more affected by long-term changes caused by precipitation,
whereas the series of growth indices were more affected by
inter-annual variability caused by temperature.
Precipitation exerted a large positive influence on cork
growth and drought was a limiting factor, indicating the importance of the water holding capacity of the soil. Precipitation
during November and December always had a positive influence on cork growth in the following year. October appeared
to be a transitional month, probably because phellogen becomes dormant at this time. Differences in precipitation between sites could account for the higher sensitivity of cork
growth to climate in trees at La Herguijuela than at Torre
Sirgada. There was more late autumn and winter precipitation
and more severe drought in the late spring at La Herguijuela
than at Torre Sirgada (Figure 2). At Torre Sirgada, cork
growth was less restricted by lack of water (Figure 4). A saturation effect of soil water content could explain the nonlinear
relationship between cork growth and precipitation during the
November to June period at this site (Figure 6c).
Figure 8. Paired relationships between growth indices and (a)
monthly mean July temperature (Tm) and (b) absolute minimum November temperature (Tmin) at La Herguijuela; and (c) mean minimum
March temperature (Ti-M) at Torre Sirgada. The goodness of fit, R 2,
and the confidence level, P, are given in each figure. In (a), the circled
points indicate the values used to fit the exponential function. Uncircled points correspond to narrow rings formed in years in which July
Tm was lower than 28 °C but precipitation was low (the narrowest one
corresponds to 1983). Narrow rings were also formed in years in
which precipitation was higher but the temperature was above the
28 °C threshold, such as in 1989 and 1992.
Temperature generally exerted a negative effect on cork
growth, which is typical for trees growing in a Mediterranean
climate. Moderately low temperatures enhanced cork growth,
except in January and February and at the onset of phellogen
activity (April to May). During this latter period, cork growth
was stimulated by an increase in temperature, but later in the
season high temperatures slowed cork growth until the beginning of autumn. The significantly negative coefficients of the
late autumn and winter temperatures (Figure 4) could be related to carbon balance, because respiration rate can exceed
photosynthetic rate at this time of year (Edwards and Hanson
1996).
At La Herguijuela, summer temperatures showed the high-
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SENSITIVITY OF CORK GROWTH TO CLIMATE
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Figure 9. Examples of the relationships between cork growth
indices (GI) and different climatic indices: (a) quotient of
precipitation from January to
June and July Tmax; (b) quotient
of precipitation from November
(t – 1) to September (t) and July
Tmax; (c) quotient of precipitation from November (t – 1) to
September (t) and July Tmax minus May mean minimum temperature (Ti-M); (d) quotient of
precipitation from January to
June and March Ti-M; (e) quotient of precipitation from November (t – 1) to September (t)
and August Tmax minus May
Ti-M; and (f) quotient of precipitation from November to September and March Ti-M. Ti-M,
mean minimum; Tmax, absolute
maximum temperature.
est correlation coefficients. This, together with the positive effect of precipitation in June and July, indicates that cork
growth was restricted by temperatures above 28 °C or by the
lack of water, or both (Figures 2 and 7). The effect of temperature was less pronounced at Torre Sirgada than at La
Herguijuela. At Torre Sirgada, cork-ring growth was controlled more by high temperatures during winter and at the beginning of the growing period (Figure 4). The positive
temperature effect observed in April at La Herguijuela was
probably equivalent to the positive effect observed in May at
Torre Sirgada. This could indicate a certain delay in the activation of the phellogen that may be partially attributable to the
higher altitude of the La Herguijuela site. A similar delay was
observed for the July and August temperatures (Figure 4).
To understand cork growth, the effects of precipitation and
temperature should be considered together (Figure 9). The
variance explained by drought indices is higher than that explained by precipitation or temperature alone, except for July
Tm, which appears to be the most restrictive factor during the
growing period at La Herguijuela (Figure 8). Multiple linear
regression analysis corroborated the general trends observed,
especially the relationship with precipitation. In years of severe summer drought, cork trees can lose all their leaves (Natividade 1950). Also, acorns can abort if temperature or precipi-
tation, or both, are unfavorable during their development period.
For the Mediterranean basin region, dendroclimatology has
been performed for beech (Gutiérrez 1988), some pine species
(Gutiérrez 1989) and a few deciduous oaks (Serre-Bachet
1982, Tessier et al. 1994). These dendroclimatological studies
have demonstrated that summer drought is the main factor
limiting wood ring growth. The wood rings of evergreen oaks
(Quercus ilex L. and Q. suber), the predominant tree species in
the Mediterranean forest communities (Specht 1988), are hard
to identify. Few dendroclimatological data are available
(Liphschitz and Lev-Yadun 1986, Zhang and Romane 1991,
Oliveira et al. 1994, E. Gutiérrez, unpublished data). These
data suggest that cambial activity is highly sensitive to summer precipitation and, as well as during the winter dormant period, can be interrupted several times during the year, resulting
in the formation of false rings. However, in semi-arid regions
dominated by extensive cork woodlands and dehesas, as for
example, certain areas in the south of the Iberian peninsula and
in northern Africa, drendrochronology of cork (suberochronology) could provide additional information. A practical
application would be for the analysis and prediction of forest
decline due to anthropogenically induced climatic change. A
detailed knowledge of how climate influences cork production
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CARITAT, GUTIÉRREZ AND MOLINAS
and quality would aid in the management of this important
Mediterranean forest resource. Furthermore, a model could be
built for a given area to predict cork growth. We could, therefore, adjust the timing of the cork-harvest years in accordance
with the growth predicted from the interannual variations of
precipitation and temperature.
Acknowledgments
Members of the Forestry Section of the Instituto para el Corcho, la
Madera y el Carbón, Junta de Extremadura, Ap. 437, E-06800
Mérida, Spain, have collaborated in the selection of the sites, in sample and data collection and discussion of the results, and should be
considered co-authors of this paper. Dr. Miguel Elena (Institute director) and Dr. Enrique Cardillo deserve particular acknowledgement.
The authors thank the owners of La Herguijuela for their kind collaboration and Dr. Emili Garcia-Berthou for his help in the preparation of
the manuscript.
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