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Annual cork-ring width variability of Quercus suber L. in relation to temperature and precipitation (Extremadura, southwestern Spain)
Pores;;~ology Management ELSEVIER
Forest Ecology and Management 86 (I 996) 113- 120
Annual cork-ring width variability of Quercus suber L. in relation to temperature and precipitation (Extremadura, southwestern Spain) A. Caritat a9* , M. Molinas a, E. Gutierrez b a Cork-Oak Laboratory, University of Girona, PI. Hospital b Department of Ecology, University of Barcelona, Au. Diagonal
6. 17071 Girona, Spain 645. 08028 Barcelona, Spain
Accepted 12 March 1996
Abstract A 14 year sequence of cork-ring width chronology is correlated with rainfall and temperature data. Cork specimens were obtained from three cork peel samplings carried out in 1989, 1991 and 1993 from a cork ‘dehesa’ in Ckeres, Spain. Average width of cork-rings varied between 2.05 and 4.37 mm. The cork-ring width chronologies of the three peel-off samplings show definite agreement patterns. Differences in ring width in years of greater and lesser growth are clearly marked. Correlation between ring width and rainfall indicates that the rain periods with the greatest influence on cork growth are those occurring from November to June, followed by those from November to September. Temperature, on the other hand, shows a negative correlation with cork growth, except during the coldest months and the months of April and September when temperature possibly has a crucial influence on phellogen activation. Keywords: Climatic fluctuations; Cork-oak; Cork growth; Cork-ring chronology; Quercus
1. Introduction
It is well known that in temperate zones many woody species form distinct annual rings of wood during the favorable growth period of the year. These records of annual growth are valuable sources of information on environmental changes (Fritts, 1976; Cook and Kairiukstis, 1990). Many Mediterranean species do not form distinct
* Corresponding author. 0378-I 127/%/$15.00 PII SO378-1
annual
tree rings
L.
and cambial activity must be followed over several years to establish the growth pattern and its relation to climatic factors. The research carried out on cambial activity by Fahn (Fahn, 1962) and Liphschitz and Lev-Yadum (Liphschitz and Lev-Yadum, 1986) has shed light on the geographical origin and the degree of adaptation of many species growing under Mediterranean climatic conditions. Quercus suber L., the cork oak, is a species adapted to Mediterranean conditions with variable cambial activity in relation to climatic factors. Ephrat (Ephrat, 1971) established that low winter temperatures and summer
Copyright 0 1996 Elsevier Science B.V. All rights reserved.
127(96)03787-5
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drought are the most important factors in controling cambial activity. However, much less attention has been paid to phellogen activity and the pattern of cork-ring formation, even though Q. saber forms annual cork-rings that can also be successfully employed in studying the response of phellogen to climate. In cork-oak, phellogen is a permanent meristematic layer that produces a phellem thick enough to be used commercially. For commercial exploitation the cork bark is removed when it measures at least 2.5 cm, resulting in peel-off turns 8-14 years apart depending on the geographical area. After each bark stripping a new phellogen is differentiated within the secondary phloem or bast and at each season of growth a new cork-ring is added to the regenerated phellem. Very little is known about the effects of climatic variability on cambial or phellogen activity in corkoak, which need not necessarily show the same pattern. Natividade (Natividade, 1950) reports data on ring width from near Evora (southern Portugal) and suggests that the phellogen rest period extends from the end of October or beginning of November until about the middle or end of April. Lombardero and Montero (Lombardero and Montero, 1980) compared cork production in successive peel-offs from ‘dehesa’ woods in Caceres (Spain). Zeraia (Zeraia, 198 1) studied relationships between phenological characteristics, production and environmental factors and their impact on cork-oak woods in Provence (France) and Algeria. Gonzalez Adrados and coworkers (Gonzalez Adrados et al., 1992; Gonzalez Adrados et al., 1993) studied geographic distribution and cork quality in Extremadura and Catalonia (Spain), with some references to ring width. More recently, Fos and Batreno (Fos and Barreno, 1994) have measured the annual growth of cork-rings in Catalonia and Valencia (Spain), reporting that differences in ring thickness could be related to the extent of the dry summer period. The aim of the present paper is to analyze the relationship between annual cork-ring width and climatic variables (monthly rainfall and temperatures) by means of dendrochronological methods (Cook and Kairiukstis, 1990). It is assumed that the series of annual cork-ring widths reflect year-to-year climatic variability and can successfully be used to find out which climatic variables are most limiting for
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cork-ring growth. The present study is based on cork samples from a ‘dehesa’ cork-oak wood in Caceres (southwestern Spain).
2. Study area
The study area is located in southwestern Spain (Caceres), where Q. suber grows naturally. The cork-oak is widely distributed in the western Mediterranean, growing only on siliceous substratum. It is less tolerant to low temperatures than Q. ifex and requires higher annual rainfall, about 600 mm. The woodlands containing this species have been managed for centuries as a multipurpose corkoak forest, ‘dehesa’, for cork production, livestock and for growing grass or wheat. Tree density per hectare is low, and trees are stripped regularly every 11 years for cork production. Cork samples were obtained from the ‘dehesa’ ‘La Herguijuela’ (Caceres) at about Y55’W 39”56’N, and 300-400 m.a.s.1. Annual rainfall over the last 20 years amounts to 598 + 219 mm, and mean annual temperature is 17 + 1.6% with a mean maximum of 44°C (August) and a minimum of 3°C (January). The climatic diagram clearly shows the Mediterranean characteristics, the highest mean temperatures are reached in the summer months when precipitation is
“C
Wll
70 -m ---CC
60
100
50
0
I-
J
FMAMJJASOND
Fig. 1. Average monthly precipitation and temperature recorded at the meteorological weather station of C.M. Torrejbn @iceres, Spain) covering the 14 year period 1979- 1992.
A. Caritat
et d/Forest
Ecology
lowest (Fig. 1). The parent soil material is formed by alluvial debris on a Miocene substratum.
3. Samples and data collection
Cork samples from three cork peel-off collections carried out in the summers of 1989, 1991 and 1993 were kindly provided by the Forestry Section of the ‘Instituto de PromociQ de1 Corcho’ (IPROCOR) in MCrida (Spain). Tree ages ranged from 150 to 170 years and tree density was 30 individuals per ha. The average tree height was 6,89 m ( + 0.95); the average breadth height diameter (DBH) was 62 cm ( k 4); the average bifurcation height was 2.47 m ( ? 0.20) and the average cork peeling height was 2.83 m ( k 0.29). From the 1993 peel-off collection, 57 cork samples from as many randomly selected cork-oak trees were obtained. Of these, 11 samples were rejected on technical grounds, and the remaining 46 samples were examined and the rings were identified and measured. From the 1989 and 1991 peel-off collections, 13 and 11 samples were selected, respectively, from among those in which cork-rings could be most clearly identified and measured. Climatic data were obtained from a neighboring meteorological weather station, C.M. Torrej6n (Ckeres) at 0.5 km from the site sampled. Complete series of precipitation and temperature recordings covering a period of 20 years were available and were checked for homogeneity.
4. Cork-ring
series and data analysis
The selected cork samples were boiled in water for about 45 min to reduce inner tension and prepare them for thin slicing the better to observe the corkrings. For each sample the total cork thickness (caliber) was measured. Cork-ring boundaries are quite clear owing to differences in the cells produced at the beginning and at the end of the growth period. In spring cells have thinner walls and are larger in diameter than those formed later in the year (Pereira et al., 1987). Rings were counted and dated, and a visual synchronization of the ring series was carried out for an accurate cross-dating of the whole series. The widest
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and narrowest rings were used as markers to identify false rings and to locate missing rings. The initial and final half rings were rejected as being related to incomplete growth periods of less than one year. Cork-ring widths were measured with a 10 X binocular microscope equipped with a micrometer scale with a precision range of 0.1 mm. For each set of samples obtained from each respective peel-off collections, ring width series were compared using multiplot representations of the data for a visual check on agreement among the curves as is usually done in dendrochronological studies (Cook and Kairiukstis, 1990). Further, correlation analysis between series was performed to verify synchronization. The chronologies showing the highest correlation coefficients were avtraged to obtain a mean chronology which in turn was used to locate double or missing rings. All the individual series showed a decreasing growth trend relative to age and they were averaged to obtain the three mean growth curves for the whole of the period studied. Finally, a unique mean growth curve was established covering a period of 14 years, from 1979 to 1992. To minimize the influence of cork age and to underscore the annual fluctuations of growth owing to climate, the mean growth curve of raw ring width data was standardized using the growth function described by Warren (Warren, 1980) Y, = atbeeC’E,
where Y, = f, E,, Y, denotes the actual measurements of ring width, ?t the estimated values, and E, the residuals or remainders, called growth indexes in dendrochronological studies. This series is assumed to be constant as regards mean and variance. The role of annual rainfall and temperature patterns in cork growth indexes was examined by means of correlation analysis. Mean, maximum and minimum monthly temperatures were correlated with a series of growth indexes as well as different combinations of periods of monthly precipitation. 5. Results and discussion 5.1. Annual cork growth
In ‘La Herquijuela’ the average cork-ring width ranges from 2.05 to 4.37 mm with a mean value of
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Table 1 Average cork-ring width in cork from the peel-off 1989, 1991 and 1993 in ‘La Herguijuela’ (Caceres, Year
Annual (n=
cork growth SD
1989
II)
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collections Spain)
(It=
SD 13)
1993
SD
(n=46)
1.24 0.94
1981 1982
3.04 3.98 2.55
1.10 1.99 0.78
3.29 3.01 2.78
1.26 0.86 0.81
3.04
1.41
4.37 4.05
1.19 1.04
3.53 3.60
1.39 1.38
3.85 4.00
0.73
2.98
0.88
2.72
1.05
3.09
1.11 1.03
3.54 3.52
1.25
3.45
1.00
1989
3.59 2.3 1
1.12 0.89 0.66
4.21 4.00 2.05
0.84 0.76 0.66
1990
2.62
0.63
2.71 2.38 2.06
0.62 0.57 0.70
1987 1988
1991
1992
113-120
(mm) 1991
3.32 2.72
1985 1986
86 (1996)
of
1979 1980
1983 1984
und Mumgement
Fig. 3. Mean annual growth curve (open circles) of cork-ring widths covering a 14 year period ( 1979- 1992). A growth -function was adjusted to detrend tire series of growth; the fitted values (tilled circles) are represented.
forest in which trees grow at higher densities. In northeast Spain, we found a mean ring width of 2.5 mm in a forest site of 400-600 trees ha-‘. In southeastern France, Zeraia (Zeraia, 1981) found values of about 0.7-0.8 mm in uncleared forests of up to 1000 tree ha- ’ . In two sites of similar tree age and density (500 trees ha-’ ) in northeast Spain (UTM: 3 1TDG) and eastern Spain (UTM: 3OSYKJ Fos and Barren0 (Fos and Barreno, 1994) report mean values of 2.9 mm and 1.6 mm, respectively; they relate these differences to the duration of the dry summer period. The mean annual cork-ring width chronologies from the three peel-off collections studied (years 1989, 1991. and 1993) are depicted in Fig. 2. The three growth curves show a clear synchronization of
n, number of samples. SD, standard deviation.
3.2 1 mm (Table 1) and cork caliber varies from 24 to 41 mm. These ring width values are similar to those reported from dehesas in southern Portugal by Natividade (Natividade, 1950) with cork specimens of 36 mm in caliber (mean ring width 3.74 mm); where he also observed rings as wide as 8.18 mm with very thick bark (caliber 58.5 mm> and also very narrow rings of 1.2 mm with thin bark (caliber 18 mm>. However, the average growth of cork-rings in the dehesa system is usually greater than in natural annual
Fig. 2. Average ammal cork-ring width curves from peel-off growth curves show very good agreement between them.
cork
growth
collections
of 1989, 1991 and 1993 in ‘La Herguijuela’
(C&ems,
Spain). The
A. Caritat
et al./Forest
Annual
Fig. 4. Annual cork-ring growth indices chronology year (t - 1) to April of the year of growth, r (tilled
Ecology
cork
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(open circles) in relation to precipitation triangles). See also Table 2.
38
c 4
cork
117
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growth/precipitations
their growth patterns. Years of maximum and minimum growth rates stand out clearly and are common to each one of them. The total period covered by the three chronologies is 14 years, from 1979 to 1992. The mean annual growth chronology for the whole period covered by the three mean series of growth rings is shown in Fig. 3, together with the fitted growth values. The percentage of variance accounted for by the growth function model is R2 = 41%. In fact, the accuracy of fit is poor, probably because the series is short. However, a certain degree of standardization is necessary to better appreciate climatic effect on bark cork-rings. The values of the parameters are a= 1.11, b=0.034, and c= -0.08. Ring
Annual
86 (1996)
accumulated
from November
width indices chronology is shown is Fig. 4 and Fig. 5. 5.2. Inji’uence of precipitation and temperature
The statistical analyses could not be as complex as they usually are in dendrochronological studies because the ring series are too short. Even so, the correlation analysis results show significant levels of confidence for a number of correlation coefficients which can be taken into consideration when making inferences about cork-ring growth in relation to climate. The correlation coefficients throughout the series
growth/max.temperatures
,
[IS
36-
T Jun
-184
I cr
-133 -1.2
34,u
- 1.1
; m 32-
-1.0
E +
of the previous
-0,9 30-
b -
-0,8 -0.7
26
Fig. 5. Annual
cork-ring
! 1978
growth
-0.6 I CO.5 1983
indices (open circles)
1988
in relation
to maximum
1993
June temperature
(filled
squares).
See also Table 3.
118
A. Caritut
Table 2 Correlation coefftcients and the accumulated periods of the year
et al./ Forest
between annual cork-ring growth indexes mean monthly precipitation for different
Period
Cork growth/ precipitation correlation coefficients 0.796 * ’ 0.487 0.3 I5 0.507 * -0.080 0.408 0.644 . 0.288 0.762 * 0.825 * * 0.852 - ’ 0.353 0.745 * *
January-June April-June July-August March-September October-December January-December April-October September-October November (previous yea&April November (previous yea&June November (previous yea&September October-December (previous year) October (previous year)-September Asterisks indicate * * P < 0.01).
Ecology
significant
statistical
differences
( _ P < 0.05,
of annual cork-ring growth indexes and rainfall, covering different periods of the year, are listed in Table 2. The highest correlation coefficients were obtained for some combinations of monthly precipitation rates throughout a whole year with periods of the year in which trees are growing (from March to October) and in which trees are dormant. This could mean that while the effect of water on current growth activity is important, so is the water that can be stored in the soil and remains available for the next period of growth. Thus, the most significant correlation coefficients are found with relation to rainfall from November of the previous year (t - 1) to September of the year of growth (1) (r = 0.852) and rainfall from November ( t - 1) to June (t) (r = 0.8251, followed by the rainfall from January (t) to June (t) ( r = 0.7961, rainfall from November (t - 1) to April (t) (r = 0.762) (Fig. 4) and rainfall from October (r - 1) to September (t) (r = 0.745). There are also high and significant correlation coefficients although somewhatlower, when considering the precipitation for the months of the growth period alone (Table 2). The correlation with rainfall from April (t) to October (t) is r = 0.644, and the correlation with rainfall from March (r) to Septem-
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86 (19961 113-120
ber ( t) is r = 0.507. When rainfall is analyzed month by month in relation to growth indexes, only January (t) and June (r) show significant correlation coefficients. According to these results January and June could be consideredkey months. On the whole, the years of greatest cork development are those with abundant precipitation during the first semesterand the last months of the previous year. This fact is clear from comparison of the climatic diagrams corresponding to the years 1989. and 1990. In 1990 there was a dry spring and high precipitation in October and November. This rainfall pattern was associated with a narrow cork-ring growth in that sameyear (1989) but had a positive effect on ring width the following year (1990). It is unknown to what extent cork-oak trees can accumulate water during the phellogen rest period for use in the next period of growth. Table 3 shows the correlation coefficients for ring-width indices and monthly mean, maximum and minimum temperatures(see also Fig. 5). In general. a negative correlation with growth indexes has been obtained for the 14 year sequencestudied. This does not apply to mean, maximum, and minimum temperature in April, to mean and minimum temperature in January and February, or to mean temperatures in September,which show positive although not signifi-
Table 3 Correlation coefficients between annual cork-ring growth and monthly mean, maximum and minimum temperatures Month
Asterisks indicate * * P < 0.01).
-.
Cork growth/temperature correlation coefficients Mean T
January February March April May June July August September October November December
indexes
Max T
0.227 0.104 0.677 + . 0.399 -0.340 -0.533 -0.377 -0.2 14 0.067 -0.626 * -0.42 I -0.429 significant
Mm ‘T
-0.240 -0.155 -0.534 0.222 -0.323 -0.591 -0.403 -0.048 -0.052 -0.570 -0.33 -0.361 statistical
a
s
* 1
differences
0.430 0.248 -(!.565 . 0.477 -031 I -0.414 .0.399 0.396 -0.023 -!,.579 * -O..W4 -0.253
-
( ’ f’ < 0.05,
A. Caritat
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cant correlation coefficients. The highest significant correlation coefficient was obtained for mean March temperatures with growth indexes, and this month maximum and minimum temperatures are also significantly related to growth. High temperatures during March might inhibit phellogen activity and have a protective effect if frosts were frequent during April, in which temperature also showed a positive correlation with growth. It could be something like a security mechanism since phellogen activity if it took place in April could have a deleterious effect. The negative correlation between temperatures and ring-width indexes during the growth period (from May to August) means that lower temperatures would be more suitable for cork-ring growth. These results also agree with the fact that atmospheric summer drought can begin in May and last until October (Fig. 1). The high significant negative correlation between October temperature and growth ring indices, could be interpreted as indicating that high temperatures do not favor the growth of cork-rings during fall, even when rainfall is high. Another possible interpretation is that high temperatures increase respiration and this probably has a negative effect on growth. The same explanation could account for the negative correlation between growth and maximum temperatures, both mean and absolute, during winter; furthermore, correlations being positive between growth and minimum temperatures during winter (Table 3). Negative correlations with temperature and positive correlations with rainfall in late spring and summer are a typical responses shown by many species growing in a Mediterranean climate (Tessier, 1986; GutiCrrez, 1988). During summer droughts, the lack of water together with high temperatures may have synergetic effects and both factors appear to be limiting. However, precipitation appears to be more limiting according to the value of the correlation coefficients and to the number of those that are significant. The effect of precipitation and temperature on the ring growth of the cork-oak suggests that this species is able to respond to the dry summer period. The cork oak’s xerophytic character is manifested in other aspects of its ecophysiological behavior (Tenhunen et al., 1984; Oliveira et al., 1992; Oliveira et al., 1994). According to Natividade (Natividade,
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86 (1996)
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119
1950) the phellogen summer rest only occurs in very dry years or in those when large-scale defoliation takes place. We are aware that statistical analysis cannot prove cause-effect relationships, but the correlations obtained between cork-ring growth and temperature (negative correlation in March, and positive in April and September) could indicate that the active period of phellogen may last from April to September. This is a period similar to that reported by Natividade (Natividade, 1950) in Portugal.
6. Conclusions Cork-ring widths of Q. suber have proved to be very sensitive to year-to-year climatic variability. The results have shown that the cork-ring growth dynamics described are also indicative of the high sensitivity of the phellogen to climatic factors, monthly rainfall and mean temperature. This is also the first time that an analysis of the relationship between climatic variables and cork-ring growth indexes has been performed. The period that has shown the highest correlation runs from November (t - I) to September (11, a period of rainfall that includes both the precipitation that falls during the growth season and the precipitation that can be stored in the soil and remains available for the next period of growth. This positive delayed effect clearly occurred in 1990. The overall effect of temperature as discussed in terms of correlation coefficients is less important than the effect of rainfall. However, temperature is a key factor limiting cork-ring formation through several specific processes: this is seen in the initiation of phellogen activity (see negative effect of March temperature), in the water stress caused by high temperatures during the growth period, and in the negative effect on growth of temperature in October, at the end of the season, when phellogen has to enter dormancy.
References Cook, E.R. and Kairiukstis, L.A., 1990. Methods drochronology. Applications in the Environmental Kluwer Academic, Dordrecht, 304 pp.
of DenSciences.
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Ephrat, Y., 197 1. Periderm development and the annual rhythm of phellogen and cambial activity in Quercu.s suber and Quercus calliprinos. M. SC. Thesis, Tel-Aviv University. Fahn, A., 1962. Xylem structure and the annual rhythm of cambial activity in woody species of the East Mediterranean regions. Int. Assoc. Wood Anat. Bull., 1961/2: 2-6. Fos, S. and Barreno, E., 1994. Crecimiento radial de1 corcho de reproduccidn de 10s alcomocales catalanes y valencianos. Sci. Gerund., 20: 5-15. Fritts, H.C., 1976. Tree Rings and Climate. Academic, New York, 576 pp. Gonzalez Adrados, J. R., Elena, R. and Tella, G., 1992. Potencialidad de1 territorio para el alcomoque en Extremadura. Sci. Gerund.. 18: 1855194. Gonzalez Adrados, J. R., Montero. G. and Ortega, C.. 1993. Caracterizacion productiva de 10s alcomocales catalanes. Investigacion Agraria. Sistemas y Recursos Forestales, Vol. 2. Instituto National de Investigaci6n y Tecnologia Agraria y Alimentaria, pp. 55-69. GutiCrrez, E., 1988. Dendroecological study of Fagus siluuticu L. in the Montseny mountains (Spain). Acta Oecologica. Oecol. Plant., 9: 301-309. Liphschitz, N. and Lev-Yadum, S., 1986. Cambial activity of evergreen and seasonal dimorphics around the Mediterranean. Int. Assoc. Wood Anat. Bull., 7: 145- 153. Lombardero, B. and Montero, G., 1980. Estudio comparative de la produccidn de corcho con tumos de descorche de 9 y 10 a.iios.
ad
Management
86 (1996)
l/3-120
An. Inst. Nat. Invest. Agrar. (Spain), Ser. Rec. Nat., 4: 165-171. Natividade, V., 1950. Subericultura. Dircc~ao Generai dos Services Florestais e Aquicolas, Lisboa. Oliveira, G., Correira, 0. A, Martins-Lou(;ao, M.A. and Catarino F. M., 1992. Water relations of cork-oak (Quercus suber I...) under natural conditions. Vegetatio, 99-100: 199-208. Oliveira, G., Correira 0. A, Martins-Loupe, M.A. and Catarino F. M.. 1994. Phenological and growth patterns of the Mediterranean oak Quercus subrr L. Trees, 9: 41-46. Pereira, H., Rosa, M.E. and Fortes, M.A.,1987. The cellular structure of cork from Quercus suber L. Int. Assoc. Wood Anat. Bull., 8: 213-218. Tenhunen, J.D.. Lange, O.L.. Gebel, J., Beyschlag, W. and Weber, J.A., 1984. Changes in photosynthetic capacity, carboxylation efficiency, and CO2 compensation point associated with midday stomata1 closure and midday depression of net CO, exchange of leaves of Quercu.\ suher. Planta, 162: 193-203 Tessier L., 1986. Approche dendroclimatologique de I’ecologie de Pinus syluestrrs L. et Quercuspubescens Wild. dans le Sud-Est de la France. Acta Oecologica. Oecol. Plant, 7: 339-355. Warren, W. G., 1980. On removing the growth trend from dendrochronological data. Tree-Ring Bull., 40: 35-44. Zeraia, L., 198 I. Essai d’interpretation comparative des don&es ecologiques, phenologiques et de production subcro-ligneuse dans les forets. These, Universite de Droit d’Economie et der Sciences d’Aix-Marseille.
Forest Ecology and Management 86 (I 996) 113- 120
Annual cork-ring width variability of Quercus suber L. in relation to temperature and precipitation (Extremadura, southwestern Spain) A. Caritat a9* , M. Molinas a, E. Gutierrez b a Cork-Oak Laboratory, University of Girona, PI. Hospital b Department of Ecology, University of Barcelona, Au. Diagonal
6. 17071 Girona, Spain 645. 08028 Barcelona, Spain
Accepted 12 March 1996
Abstract A 14 year sequence of cork-ring width chronology is correlated with rainfall and temperature data. Cork specimens were obtained from three cork peel samplings carried out in 1989, 1991 and 1993 from a cork ‘dehesa’ in Ckeres, Spain. Average width of cork-rings varied between 2.05 and 4.37 mm. The cork-ring width chronologies of the three peel-off samplings show definite agreement patterns. Differences in ring width in years of greater and lesser growth are clearly marked. Correlation between ring width and rainfall indicates that the rain periods with the greatest influence on cork growth are those occurring from November to June, followed by those from November to September. Temperature, on the other hand, shows a negative correlation with cork growth, except during the coldest months and the months of April and September when temperature possibly has a crucial influence on phellogen activation. Keywords: Climatic fluctuations; Cork-oak; Cork growth; Cork-ring chronology; Quercus
1. Introduction
It is well known that in temperate zones many woody species form distinct annual rings of wood during the favorable growth period of the year. These records of annual growth are valuable sources of information on environmental changes (Fritts, 1976; Cook and Kairiukstis, 1990). Many Mediterranean species do not form distinct
* Corresponding author. 0378-I 127/%/$15.00 PII SO378-1
annual
tree rings
L.
and cambial activity must be followed over several years to establish the growth pattern and its relation to climatic factors. The research carried out on cambial activity by Fahn (Fahn, 1962) and Liphschitz and Lev-Yadum (Liphschitz and Lev-Yadum, 1986) has shed light on the geographical origin and the degree of adaptation of many species growing under Mediterranean climatic conditions. Quercus suber L., the cork oak, is a species adapted to Mediterranean conditions with variable cambial activity in relation to climatic factors. Ephrat (Ephrat, 1971) established that low winter temperatures and summer
Copyright 0 1996 Elsevier Science B.V. All rights reserved.
127(96)03787-5
suber
114
A. Caritut
et al./
Forest
Ecology
drought are the most important factors in controling cambial activity. However, much less attention has been paid to phellogen activity and the pattern of cork-ring formation, even though Q. saber forms annual cork-rings that can also be successfully employed in studying the response of phellogen to climate. In cork-oak, phellogen is a permanent meristematic layer that produces a phellem thick enough to be used commercially. For commercial exploitation the cork bark is removed when it measures at least 2.5 cm, resulting in peel-off turns 8-14 years apart depending on the geographical area. After each bark stripping a new phellogen is differentiated within the secondary phloem or bast and at each season of growth a new cork-ring is added to the regenerated phellem. Very little is known about the effects of climatic variability on cambial or phellogen activity in corkoak, which need not necessarily show the same pattern. Natividade (Natividade, 1950) reports data on ring width from near Evora (southern Portugal) and suggests that the phellogen rest period extends from the end of October or beginning of November until about the middle or end of April. Lombardero and Montero (Lombardero and Montero, 1980) compared cork production in successive peel-offs from ‘dehesa’ woods in Caceres (Spain). Zeraia (Zeraia, 198 1) studied relationships between phenological characteristics, production and environmental factors and their impact on cork-oak woods in Provence (France) and Algeria. Gonzalez Adrados and coworkers (Gonzalez Adrados et al., 1992; Gonzalez Adrados et al., 1993) studied geographic distribution and cork quality in Extremadura and Catalonia (Spain), with some references to ring width. More recently, Fos and Batreno (Fos and Barreno, 1994) have measured the annual growth of cork-rings in Catalonia and Valencia (Spain), reporting that differences in ring thickness could be related to the extent of the dry summer period. The aim of the present paper is to analyze the relationship between annual cork-ring width and climatic variables (monthly rainfall and temperatures) by means of dendrochronological methods (Cook and Kairiukstis, 1990). It is assumed that the series of annual cork-ring widths reflect year-to-year climatic variability and can successfully be used to find out which climatic variables are most limiting for
und
Munugement
86 (19961
113-120
cork-ring growth. The present study is based on cork samples from a ‘dehesa’ cork-oak wood in Caceres (southwestern Spain).
2. Study area
The study area is located in southwestern Spain (Caceres), where Q. suber grows naturally. The cork-oak is widely distributed in the western Mediterranean, growing only on siliceous substratum. It is less tolerant to low temperatures than Q. ifex and requires higher annual rainfall, about 600 mm. The woodlands containing this species have been managed for centuries as a multipurpose corkoak forest, ‘dehesa’, for cork production, livestock and for growing grass or wheat. Tree density per hectare is low, and trees are stripped regularly every 11 years for cork production. Cork samples were obtained from the ‘dehesa’ ‘La Herguijuela’ (Caceres) at about Y55’W 39”56’N, and 300-400 m.a.s.1. Annual rainfall over the last 20 years amounts to 598 + 219 mm, and mean annual temperature is 17 + 1.6% with a mean maximum of 44°C (August) and a minimum of 3°C (January). The climatic diagram clearly shows the Mediterranean characteristics, the highest mean temperatures are reached in the summer months when precipitation is
“C
Wll
70 -m ---CC
60
100
50
0
I-
J
FMAMJJASOND
Fig. 1. Average monthly precipitation and temperature recorded at the meteorological weather station of C.M. Torrejbn @iceres, Spain) covering the 14 year period 1979- 1992.
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lowest (Fig. 1). The parent soil material is formed by alluvial debris on a Miocene substratum.
3. Samples and data collection
Cork samples from three cork peel-off collections carried out in the summers of 1989, 1991 and 1993 were kindly provided by the Forestry Section of the ‘Instituto de PromociQ de1 Corcho’ (IPROCOR) in MCrida (Spain). Tree ages ranged from 150 to 170 years and tree density was 30 individuals per ha. The average tree height was 6,89 m ( + 0.95); the average breadth height diameter (DBH) was 62 cm ( k 4); the average bifurcation height was 2.47 m ( ? 0.20) and the average cork peeling height was 2.83 m ( k 0.29). From the 1993 peel-off collection, 57 cork samples from as many randomly selected cork-oak trees were obtained. Of these, 11 samples were rejected on technical grounds, and the remaining 46 samples were examined and the rings were identified and measured. From the 1989 and 1991 peel-off collections, 13 and 11 samples were selected, respectively, from among those in which cork-rings could be most clearly identified and measured. Climatic data were obtained from a neighboring meteorological weather station, C.M. Torrej6n (Ckeres) at 0.5 km from the site sampled. Complete series of precipitation and temperature recordings covering a period of 20 years were available and were checked for homogeneity.
4. Cork-ring
series and data analysis
The selected cork samples were boiled in water for about 45 min to reduce inner tension and prepare them for thin slicing the better to observe the corkrings. For each sample the total cork thickness (caliber) was measured. Cork-ring boundaries are quite clear owing to differences in the cells produced at the beginning and at the end of the growth period. In spring cells have thinner walls and are larger in diameter than those formed later in the year (Pereira et al., 1987). Rings were counted and dated, and a visual synchronization of the ring series was carried out for an accurate cross-dating of the whole series. The widest
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and narrowest rings were used as markers to identify false rings and to locate missing rings. The initial and final half rings were rejected as being related to incomplete growth periods of less than one year. Cork-ring widths were measured with a 10 X binocular microscope equipped with a micrometer scale with a precision range of 0.1 mm. For each set of samples obtained from each respective peel-off collections, ring width series were compared using multiplot representations of the data for a visual check on agreement among the curves as is usually done in dendrochronological studies (Cook and Kairiukstis, 1990). Further, correlation analysis between series was performed to verify synchronization. The chronologies showing the highest correlation coefficients were avtraged to obtain a mean chronology which in turn was used to locate double or missing rings. All the individual series showed a decreasing growth trend relative to age and they were averaged to obtain the three mean growth curves for the whole of the period studied. Finally, a unique mean growth curve was established covering a period of 14 years, from 1979 to 1992. To minimize the influence of cork age and to underscore the annual fluctuations of growth owing to climate, the mean growth curve of raw ring width data was standardized using the growth function described by Warren (Warren, 1980) Y, = atbeeC’E,
where Y, = f, E,, Y, denotes the actual measurements of ring width, ?t the estimated values, and E, the residuals or remainders, called growth indexes in dendrochronological studies. This series is assumed to be constant as regards mean and variance. The role of annual rainfall and temperature patterns in cork growth indexes was examined by means of correlation analysis. Mean, maximum and minimum monthly temperatures were correlated with a series of growth indexes as well as different combinations of periods of monthly precipitation. 5. Results and discussion 5.1. Annual cork growth
In ‘La Herquijuela’ the average cork-ring width ranges from 2.05 to 4.37 mm with a mean value of
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Table 1 Average cork-ring width in cork from the peel-off 1989, 1991 and 1993 in ‘La Herguijuela’ (Caceres, Year
Annual (n=
cork growth SD
1989
II)
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collections Spain)
(It=
SD 13)
1993
SD
(n=46)
1.24 0.94
1981 1982
3.04 3.98 2.55
1.10 1.99 0.78
3.29 3.01 2.78
1.26 0.86 0.81
3.04
1.41
4.37 4.05
1.19 1.04
3.53 3.60
1.39 1.38
3.85 4.00
0.73
2.98
0.88
2.72
1.05
3.09
1.11 1.03
3.54 3.52
1.25
3.45
1.00
1989
3.59 2.3 1
1.12 0.89 0.66
4.21 4.00 2.05
0.84 0.76 0.66
1990
2.62
0.63
2.71 2.38 2.06
0.62 0.57 0.70
1987 1988
1991
1992
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(mm) 1991
3.32 2.72
1985 1986
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of
1979 1980
1983 1984
und Mumgement
Fig. 3. Mean annual growth curve (open circles) of cork-ring widths covering a 14 year period ( 1979- 1992). A growth -function was adjusted to detrend tire series of growth; the fitted values (tilled circles) are represented.
forest in which trees grow at higher densities. In northeast Spain, we found a mean ring width of 2.5 mm in a forest site of 400-600 trees ha-‘. In southeastern France, Zeraia (Zeraia, 1981) found values of about 0.7-0.8 mm in uncleared forests of up to 1000 tree ha- ’ . In two sites of similar tree age and density (500 trees ha-’ ) in northeast Spain (UTM: 3 1TDG) and eastern Spain (UTM: 3OSYKJ Fos and Barren0 (Fos and Barreno, 1994) report mean values of 2.9 mm and 1.6 mm, respectively; they relate these differences to the duration of the dry summer period. The mean annual cork-ring width chronologies from the three peel-off collections studied (years 1989, 1991. and 1993) are depicted in Fig. 2. The three growth curves show a clear synchronization of
n, number of samples. SD, standard deviation.
3.2 1 mm (Table 1) and cork caliber varies from 24 to 41 mm. These ring width values are similar to those reported from dehesas in southern Portugal by Natividade (Natividade, 1950) with cork specimens of 36 mm in caliber (mean ring width 3.74 mm); where he also observed rings as wide as 8.18 mm with very thick bark (caliber 58.5 mm> and also very narrow rings of 1.2 mm with thin bark (caliber 18 mm>. However, the average growth of cork-rings in the dehesa system is usually greater than in natural annual
Fig. 2. Average ammal cork-ring width curves from peel-off growth curves show very good agreement between them.
cork
growth
collections
of 1989, 1991 and 1993 in ‘La Herguijuela’
(C&ems,
Spain). The
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Annual
Fig. 4. Annual cork-ring growth indices chronology year (t - 1) to April of the year of growth, r (tilled
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cork
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(open circles) in relation to precipitation triangles). See also Table 2.
38
c 4
cork
117
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growth/precipitations
their growth patterns. Years of maximum and minimum growth rates stand out clearly and are common to each one of them. The total period covered by the three chronologies is 14 years, from 1979 to 1992. The mean annual growth chronology for the whole period covered by the three mean series of growth rings is shown in Fig. 3, together with the fitted growth values. The percentage of variance accounted for by the growth function model is R2 = 41%. In fact, the accuracy of fit is poor, probably because the series is short. However, a certain degree of standardization is necessary to better appreciate climatic effect on bark cork-rings. The values of the parameters are a= 1.11, b=0.034, and c= -0.08. Ring
Annual
86 (1996)
accumulated
from November
width indices chronology is shown is Fig. 4 and Fig. 5. 5.2. Inji’uence of precipitation and temperature
The statistical analyses could not be as complex as they usually are in dendrochronological studies because the ring series are too short. Even so, the correlation analysis results show significant levels of confidence for a number of correlation coefficients which can be taken into consideration when making inferences about cork-ring growth in relation to climate. The correlation coefficients throughout the series
growth/max.temperatures
,
[IS
36-
T Jun
-184
I cr
-133 -1.2
34,u
- 1.1
; m 32-
-1.0
E +
of the previous
-0,9 30-
b -
-0,8 -0.7
26
Fig. 5. Annual
cork-ring
! 1978
growth
-0.6 I CO.5 1983
indices (open circles)
1988
in relation
to maximum
1993
June temperature
(filled
squares).
See also Table 3.
118
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Table 2 Correlation coefftcients and the accumulated periods of the year
et al./ Forest
between annual cork-ring growth indexes mean monthly precipitation for different
Period
Cork growth/ precipitation correlation coefficients 0.796 * ’ 0.487 0.3 I5 0.507 * -0.080 0.408 0.644 . 0.288 0.762 * 0.825 * * 0.852 - ’ 0.353 0.745 * *
January-June April-June July-August March-September October-December January-December April-October September-October November (previous yea&April November (previous yea&June November (previous yea&September October-December (previous year) October (previous year)-September Asterisks indicate * * P < 0.01).
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significant
statistical
differences
( _ P < 0.05,
of annual cork-ring growth indexes and rainfall, covering different periods of the year, are listed in Table 2. The highest correlation coefficients were obtained for some combinations of monthly precipitation rates throughout a whole year with periods of the year in which trees are growing (from March to October) and in which trees are dormant. This could mean that while the effect of water on current growth activity is important, so is the water that can be stored in the soil and remains available for the next period of growth. Thus, the most significant correlation coefficients are found with relation to rainfall from November of the previous year (t - 1) to September of the year of growth (1) (r = 0.852) and rainfall from November ( t - 1) to June (t) (r = 0.8251, followed by the rainfall from January (t) to June (t) ( r = 0.7961, rainfall from November (t - 1) to April (t) (r = 0.762) (Fig. 4) and rainfall from October (r - 1) to September (t) (r = 0.745). There are also high and significant correlation coefficients although somewhatlower, when considering the precipitation for the months of the growth period alone (Table 2). The correlation with rainfall from April (t) to October (t) is r = 0.644, and the correlation with rainfall from March (r) to Septem-
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86 (19961 113-120
ber ( t) is r = 0.507. When rainfall is analyzed month by month in relation to growth indexes, only January (t) and June (r) show significant correlation coefficients. According to these results January and June could be consideredkey months. On the whole, the years of greatest cork development are those with abundant precipitation during the first semesterand the last months of the previous year. This fact is clear from comparison of the climatic diagrams corresponding to the years 1989. and 1990. In 1990 there was a dry spring and high precipitation in October and November. This rainfall pattern was associated with a narrow cork-ring growth in that sameyear (1989) but had a positive effect on ring width the following year (1990). It is unknown to what extent cork-oak trees can accumulate water during the phellogen rest period for use in the next period of growth. Table 3 shows the correlation coefficients for ring-width indices and monthly mean, maximum and minimum temperatures(see also Fig. 5). In general. a negative correlation with growth indexes has been obtained for the 14 year sequencestudied. This does not apply to mean, maximum, and minimum temperature in April, to mean and minimum temperature in January and February, or to mean temperatures in September,which show positive although not signifi-
Table 3 Correlation coefficients between annual cork-ring growth and monthly mean, maximum and minimum temperatures Month
Asterisks indicate * * P < 0.01).
-.
Cork growth/temperature correlation coefficients Mean T
January February March April May June July August September October November December
indexes
Max T
0.227 0.104 0.677 + . 0.399 -0.340 -0.533 -0.377 -0.2 14 0.067 -0.626 * -0.42 I -0.429 significant
Mm ‘T
-0.240 -0.155 -0.534 0.222 -0.323 -0.591 -0.403 -0.048 -0.052 -0.570 -0.33 -0.361 statistical
a
s
* 1
differences
0.430 0.248 -(!.565 . 0.477 -031 I -0.414 .0.399 0.396 -0.023 -!,.579 * -O..W4 -0.253
-
( ’ f’ < 0.05,
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cant correlation coefficients. The highest significant correlation coefficient was obtained for mean March temperatures with growth indexes, and this month maximum and minimum temperatures are also significantly related to growth. High temperatures during March might inhibit phellogen activity and have a protective effect if frosts were frequent during April, in which temperature also showed a positive correlation with growth. It could be something like a security mechanism since phellogen activity if it took place in April could have a deleterious effect. The negative correlation between temperatures and ring-width indexes during the growth period (from May to August) means that lower temperatures would be more suitable for cork-ring growth. These results also agree with the fact that atmospheric summer drought can begin in May and last until October (Fig. 1). The high significant negative correlation between October temperature and growth ring indices, could be interpreted as indicating that high temperatures do not favor the growth of cork-rings during fall, even when rainfall is high. Another possible interpretation is that high temperatures increase respiration and this probably has a negative effect on growth. The same explanation could account for the negative correlation between growth and maximum temperatures, both mean and absolute, during winter; furthermore, correlations being positive between growth and minimum temperatures during winter (Table 3). Negative correlations with temperature and positive correlations with rainfall in late spring and summer are a typical responses shown by many species growing in a Mediterranean climate (Tessier, 1986; GutiCrrez, 1988). During summer droughts, the lack of water together with high temperatures may have synergetic effects and both factors appear to be limiting. However, precipitation appears to be more limiting according to the value of the correlation coefficients and to the number of those that are significant. The effect of precipitation and temperature on the ring growth of the cork-oak suggests that this species is able to respond to the dry summer period. The cork oak’s xerophytic character is manifested in other aspects of its ecophysiological behavior (Tenhunen et al., 1984; Oliveira et al., 1992; Oliveira et al., 1994). According to Natividade (Natividade,
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86 (1996)
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119
1950) the phellogen summer rest only occurs in very dry years or in those when large-scale defoliation takes place. We are aware that statistical analysis cannot prove cause-effect relationships, but the correlations obtained between cork-ring growth and temperature (negative correlation in March, and positive in April and September) could indicate that the active period of phellogen may last from April to September. This is a period similar to that reported by Natividade (Natividade, 1950) in Portugal.
6. Conclusions Cork-ring widths of Q. suber have proved to be very sensitive to year-to-year climatic variability. The results have shown that the cork-ring growth dynamics described are also indicative of the high sensitivity of the phellogen to climatic factors, monthly rainfall and mean temperature. This is also the first time that an analysis of the relationship between climatic variables and cork-ring growth indexes has been performed. The period that has shown the highest correlation runs from November (t - I) to September (11, a period of rainfall that includes both the precipitation that falls during the growth season and the precipitation that can be stored in the soil and remains available for the next period of growth. This positive delayed effect clearly occurred in 1990. The overall effect of temperature as discussed in terms of correlation coefficients is less important than the effect of rainfall. However, temperature is a key factor limiting cork-ring formation through several specific processes: this is seen in the initiation of phellogen activity (see negative effect of March temperature), in the water stress caused by high temperatures during the growth period, and in the negative effect on growth of temperature in October, at the end of the season, when phellogen has to enter dormancy.
References Cook, E.R. and Kairiukstis, L.A., 1990. Methods drochronology. Applications in the Environmental Kluwer Academic, Dordrecht, 304 pp.
of DenSciences.
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et al./Forrst
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Ephrat, Y., 197 1. Periderm development and the annual rhythm of phellogen and cambial activity in Quercu.s suber and Quercus calliprinos. M. SC. Thesis, Tel-Aviv University. Fahn, A., 1962. Xylem structure and the annual rhythm of cambial activity in woody species of the East Mediterranean regions. Int. Assoc. Wood Anat. Bull., 1961/2: 2-6. Fos, S. and Barreno, E., 1994. Crecimiento radial de1 corcho de reproduccidn de 10s alcomocales catalanes y valencianos. Sci. Gerund., 20: 5-15. Fritts, H.C., 1976. Tree Rings and Climate. Academic, New York, 576 pp. Gonzalez Adrados, J. R., Elena, R. and Tella, G., 1992. Potencialidad de1 territorio para el alcomoque en Extremadura. Sci. Gerund.. 18: 1855194. Gonzalez Adrados, J. R., Montero. G. and Ortega, C.. 1993. Caracterizacion productiva de 10s alcomocales catalanes. Investigacion Agraria. Sistemas y Recursos Forestales, Vol. 2. Instituto National de Investigaci6n y Tecnologia Agraria y Alimentaria, pp. 55-69. GutiCrrez, E., 1988. Dendroecological study of Fagus siluuticu L. in the Montseny mountains (Spain). Acta Oecologica. Oecol. Plant., 9: 301-309. Liphschitz, N. and Lev-Yadum, S., 1986. Cambial activity of evergreen and seasonal dimorphics around the Mediterranean. Int. Assoc. Wood Anat. Bull., 7: 145- 153. Lombardero, B. and Montero, G., 1980. Estudio comparative de la produccidn de corcho con tumos de descorche de 9 y 10 a.iios.
ad
Management
86 (1996)
l/3-120
An. Inst. Nat. Invest. Agrar. (Spain), Ser. Rec. Nat., 4: 165-171. Natividade, V., 1950. Subericultura. Dircc~ao Generai dos Services Florestais e Aquicolas, Lisboa. Oliveira, G., Correira, 0. A, Martins-Lou(;ao, M.A. and Catarino F. M., 1992. Water relations of cork-oak (Quercus suber I...) under natural conditions. Vegetatio, 99-100: 199-208. Oliveira, G., Correira 0. A, Martins-Loupe, M.A. and Catarino F. M.. 1994. Phenological and growth patterns of the Mediterranean oak Quercus subrr L. Trees, 9: 41-46. Pereira, H., Rosa, M.E. and Fortes, M.A.,1987. The cellular structure of cork from Quercus suber L. Int. Assoc. Wood Anat. Bull., 8: 213-218. Tenhunen, J.D.. Lange, O.L.. Gebel, J., Beyschlag, W. and Weber, J.A., 1984. Changes in photosynthetic capacity, carboxylation efficiency, and CO2 compensation point associated with midday stomata1 closure and midday depression of net CO, exchange of leaves of Quercu.\ suher. Planta, 162: 193-203 Tessier L., 1986. Approche dendroclimatologique de I’ecologie de Pinus syluestrrs L. et Quercuspubescens Wild. dans le Sud-Est de la France. Acta Oecologica. Oecol. Plant, 7: 339-355. Warren, W. G., 1980. On removing the growth trend from dendrochronological data. Tree-Ring Bull., 40: 35-44. Zeraia, L., 198 I. Essai d’interpretation comparative des don&es ecologiques, phenologiques et de production subcro-ligneuse dans les forets. These, Universite de Droit d’Economie et der Sciences d’Aix-Marseille.