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Relationships between climate and double rings in Quercus ilex from northeast Spain F. Campelo, E. Gutie´rrez, M. Ribas, C. Nabais, and H. Freitas
Abstract: The influence of climatic factors on tree-ring width and the formation of double rings was studied in Quercus ilex L. growing in a coppice stand left unmanaged for 22 years. Ten trees were felled and discs were taken every 30 cm from bole and dominant branches. Dendrometer bands were installed on 10 nearby trees and the data recorded were used to confirm the accuracy of our tree-ring identification. They were also used to relate the seasonal radial growth pattern to double-ring formation. Double rings were frequent and occurred consistently along the stem. Two types of double rings could be recognized according to their width: type I, with the extra growth band accounting for approximately 50% of the tree ring; and type II, with a narrow extra growth band. Type I double rings were formed when approximately 1/2 of the growing-season precipitation occurred during the second growth period of the season and after the summer drought. Type II double rings occurred when approximately 1/3 of the precipitation in the growing season occurred after the summer drought. The formation of double rings was triggered by rainfall in summer and the extra growth-band width was related to summer and autumn environmental conditions. Double rings in Q. ilex can potentially be used in dendroclimatological studies, as they are formed in response to climatic conditions within the growing season. Re´sume´ : L’influence des facteurs climatiques sur la largeur des cernes annuels et la formation des cernes annuels doubles ont e´te´ e´tudie´s chez Quercus ilex L. croissant en taillis non ame´nage´ depuis 22 ans. Dix arbres ont e´te´ abattus et des rondelles ont e´te´ pre´leve´es a` tous les 30 cm sur le tronc et les branches principales. Des bandes-verniers ont e´te´ installe´es sur 10 arbres voisins et les donne´es enregistre´es par ces bandes ont e´te´ utilise´es pour confirmer la justesse de notre identification des cernes annuels. Elles ont aussi e´te´ utilise´es pour relier le patron saisonnier de croissance radiale avec la formation de cernes annuels doubles. Les cernes annuels doubles e´taient fre´quents et apparaissaient re´gulie`rement le long du tronc. Deux types de cernes annuels doubles pouvaient eˆtre identifie´s selon leur largeur : le type I, dont la bande de croissance additionnelle repre´sente environ 50 % du cerne annuel et le type II, caracte´rise´ par une e´troite bande de croissance additionnelle. Les cernes doubles de type I e´taient forme´s lorsque environ 1/2 des pre´cipitations de la saison de croissance survenait durant la seconde pe´riode de croissance et apre`s la se´cheresse estivale. Les cernes doubles de type II apparaissaient lorsque environ 1/3 des pre´cipitations de la saison de croissance survenait apre`s la se´cheresse estivale. La formation de cernes annuels doubles e´tait de´clenche´e par les pre´cipitations estivales et la largeur de la bande de croissance additionnelle e´tait relie´e aux conditions environnementales durant l’e´te´ et l’automne. Les cernes annuels doubles chez Q. ilex pourraient possiblement eˆtre utilise´s dans des e´tudes dendroclimatologiques puisqu’ils sont forme´s en re´ponse aux conditions climatiques durant la saison de croissance. [Traduit par la Re´daction]
Introduction In Mediterranean areas, cold winters and summer droughts are the main factors limiting plant growth (Mitrakos 1980; Terradas and Save´ 1992). Quercus ilex L. is a deep-rooted evergreen sclerophyllous species distributed widely in the Mediterranean basin (Barbero et al. 1992). It is a drought-tolerant species (Lo Gullo and Salleo 1993; Tognetti et al. 1998), and its intrinsic growth strategy prioritizes water-saving over carbon uptake (Serrano and Pen˜uelas Received 24 October 2006. Accepted 23 February 2007. Published on the NRC Research Press Web site at cjfr.nrc.ca on 18 October 2007. F. Campelo,1 C. Nabais, and H. Freitas. Centro de Ecologia Funcional, Departamento de Botaˆnica, Universidade de Coimbra, 3001-456 Coimbra, Portugal. E. Gutie´rrez and M. Ribas. Departament d’Ecologia, Facultat de Biologia, Universitat de Barcelona, Avenida Diagonal, 645, 08028 Barcelona, Spain. 1Corresponding
author (e-mail:
[email protected]).
Can. J. For. Res. 37: 1915–1923 (2007)
2005). Quercus ilex reduces stomatal conductance under drought conditions, (Save´ et al. 1999; Infante et al. 2003; Pesoli et al. 2003), under moderate water stress (Infante et al. 1997, 1999), or as a response to decreased water potential (Serrano and Pen˜uelas 2005). The morphological traits of its leaves are known to vary according to water availability. For instance, high leaf-tissue density, high leaf thickness, and low leaf area are advantageous in evergreen sclerophyllous species because they reduce water loss by transpiration during summer (Castro-Dı´ez et al. 1997, 1998; Gratani and Bombelli 1999; Sabate´ et al. 1999; Werner et al. 1999). Yet the response of anatomical traits to water constraints within the annual tree ring is less evident. It is common knowledge that Mediterranean tree species form growth rings, but ring boundaries are not always welldefined and the seasonal cambial growth pattern is not fully understood (Cherubini et al. 2003). Moreover, some tree species that grow in a Mediterranean climate show a bimodal growth pattern and therefore produce double rings in some years, making the correct dating of their growth rings extremely difficult. Wood-density fluctuations (double rings)
doi:10.1139/X07-050
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Material and methods Study area The study area is a coppice stand located in an interior valley of the Garraf karstic mountains (41820’26@N, 01850’38@E, 300 m a.s.l.) in the central Mediterranean coastal ranges and plains of Garraf and Ole`rdola Natural Park (northeast Spain). The climate is typically Mediterranean, with a mean annual temperature of 13.4 8C and mean annual precipitation of 659.9 mm (1974–2004) with peaks in spring and autumn (Fig. 1). The dry period usually extends from June to August, but both the amount and the seasonal distribution of precipitation vary significantly. Monthly values for precipitation (sum) and temperature (mean) were obtained from the nearest (8 km) meteorological station, at Begues. The current vegetation cover is about 95% and is dominated by evergreen, sclerophyllous shrublands approximately 1.5 m high, and emerging Pinus halepensis P. Mill. and Q. ilex up to 5 m high. Quercus ilex resprouted after a fire in 1982 (Lloret et al. 2003) and is more abundant on north-facing slopes. Multistemmed Q. ilex trees, which indicate a resprout origin, are dominant in the study area. Tree-ring data Ten Q. ilex trees were felled in the study area. One of these trees was cut in 2004 for preliminary investigation, and the remaining trees were cut in 2005. The height of the study trees was 3.9 ± 0.9 m (mean ± SD). Cross sections were taken every 30 cm from bole and dominant branches. Discs with a diameter 90 cm) sections. Lower section
Middle section
Upper section
Chronology length No. of trees No. of radii Mean Median Mean sensitivity Standard deviation Skewness Kurtosis First-order autocorrelation Common interval analysis No. of trees No. of radii Signal-to-noise ratio Variance of first PC (%) EPS
Raw 1984–2004 10 20 1.85 1.76 0.31 0.61 1.04 1.09 0.15 1985–2004 9 18 6.86 50.23 0.87
Standard 1984–2004 10 20 0.99 0.95 0.29 0.30 0.55 0.38 0.20 1985–2004 9 18 11.98 61.50 0.92
Raw 1984–2004 10 20 1.49 1.40 0.28 0.54 1.22 1.48 0.29 1987–2004 9 18 10.18 58.85 0.91
Standard 1984–2004 10 20 1.01 1.00 0.29 0.33 0.77 1.01 0.19 1987–2004 9 18 14.17 65.35 0.93
Raw 1985–2004 10 42 1.43 1.46 0.30 0.46 0.44 1.08 0.30 1990–2004 8 14 8.15 58.30 0.89
Standard 1985–2004 10 42 0.97 0.98 0.27 0.25 0.26 0.77 0.15 1990–2004 8 14 11.25 63.92 0.92
Mean correlation Among all radii Between trees Within trees
0.44 0.43 0.62
0.58 0.57 0.73
0.55 0.53 0.83
0.63 0.61 0.85
0.53 0.51 0.84
0.61 0.58 0.82
Note: PC, principal component; EPS, expressed population signal.
cooler. In November, temperature had a positive effect on tree-ring growth. The double rings were distinguished macroscopically from true annual rings. Of the 1426 tree rings examined, 676 displayed double rings. Double rings were not detected
in 1997, whilst in 1984 and 1995 all studied samples exhibited double rings. Two types of double rings were identified in Q. ilex. Type I, characterized by a large extra band of xylem, accounted for approximately 50% of the true tree rings (1995 in Fig. 2). Type II was characterized by a small extra #
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1919 Table 2. Pearson’s correlation coefficients between each of the six chronologies and the different sampling heights. Raw ring-width chronology
Standard chronology
Lower section Raw ring-width chronology Lower section — Middle section — Upper section — Standard chronology Lower section — Middle section — Upper section —
Middle section
Upper section
Lower section
Middle section
Upper section
0.95 — —
0.82 0.84 —
0.95 0.91 0.75
0.95 0.95 0.81
0.87 0.87 0.80
— — —
— — —
0.98 — —
0.93 0.95 —
— — —
Note: Correlations are calculated over the common interval 1985–2004. All correlations are significant at the 99% confidence level.
Fig. 3. Raw ring-width (thick line) and standard (thin line) chronologies of Quercus ilex. The broken line represents the number of discs used.
Table 3. General statistics of the raw ring-width and standard chronologies of Quercus ilex. Study area chronology
1
1
0 1985
1990
1995
2000
100 75 50 25 0
Sample depth
2
Tree-ring index
Tree-ring width (mm)
3
2005
band of xylem at the end of the true ring (1996 in Fig. 2). Because f values were similar at different heights (lower, middle, and upper sections; Fig. 6), further analyses were done without considering the height position. Greater amounts of precipitation in August led to a higher frequency of double-ring formation in Q. ilex. The temperature in August and September was negatively correlated with doublering formation (Fig. 7). The highest F value occurred in 1995, when all samples exhibited extra growth bands (88% type I). In 1996, all double rings were type II. The type of double ring was tentatively correlated with rainfall and the radial growth pattern of the corresponding year (Fig. 8). Radial increment was first perceptible in approximately April, as recorded by dendrometers. The largest radial increment occurred in April and May. During the summer drought, the radial increment either slowed down (1996) or halted completely (1995). After the summer drought, the favourable climatic conditions allow cambial activity to resume, which results in a second growth period in the season. In 1995 and 1996, an extra growth band was formed during this second growth period. According to the dendrometer data, in 1995 approximately 50% of the radial growth took place after the summer drought, while in 1996 only approximately 20% of the radial growth occurred during the second growth peak.
Chronology length No. of trees No. of radii Mean Median Mean sensitivity Standard deviation Skewness Kurtosis First-order autocorrelation Common interval analysis No. of trees No. of radii Signal-to-noise ratio Variance of first PC (%) EPS
Raw ring-width 1984–2004 10 82 1.58 1.55 0.28 0.53 1.13 1.74 0.24 1984–2003 10 20 8.67 52.50 0.90
Standard 1984–2004 10 82 1.00 0.95 0.28 0.28 0.48 0.62 0.16 1984–2003 10 20 13.31 61.60 0.93
Mean correlation Among all radii Between trees Within trees
0.47 0.46 0.60
0.58 0.57 0.69
Note: PC, principal component; EPS, expressed population signal.
The extra growth-band width was proportional to the radial growth detected by the dendrometers.
Discussion Six event years, that is, years with narrow (e.g., 1987, 1994, 1997, and 2001) or wide rings (e.g., 1992 and 1996), were identified and used to synchronize all studied Q. ilex discs. Tree-ring identification was particularly difficult on very short radii, where a lot of wedging rings occurred; for this reason, the longest possible radius was used. The occurrence of wedging and double rings emphasizes the necessity of working with cross sections (De´tienne 1989; Worbes 1995; Cherubini et al. 2003). Good synchronization among discs from the same tree and from different trees, the concurrence of narrow tree rings and dry-summer years, and #
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Can. J. For. Res. Vol. 37, 2007
3.0
Tree-ring width (mm)
2.5
2.0
1.5
1.0
Fig. 6. Stabilized frequency of double rings (f) at the three height categories in relation to calendar years. 5
Stabilized frequency of double rings [f=Fn0.5]
Fig. 4. Tree-ring widths obtained by two different methods. The thin line shows tree-ring widths measured on discs from the middle section (60–90 cm) and the thick line represents dendrometer measurements. The tree-ring width is related to the tree-ring growth measured by dendrometers (r = 0.75, p < 0.01).
upper section middle section lower section
4
3
2
1
0
0.5
1985
1985
1990
1995
2000
2005
Fig. 5. Pearson’s correlation coefficients between the standard chronology and monthly climatic data (mean temperature and total precipitation) for the period 1984–2004. Broken lines are significant thresholds for p < 0.05. The bars on the right represent the seasonal climatic coefficients (wi, winter (January, February, and March); sp, spring (April, May, and June); su, summer (July, August, and September); and au, autumn (October, November, and December)).*, p < 0.05; **, p < 0.01. 0.8 0.6
Temperature Precipitation
2000
2005
0.8 0.6
Temperature Precipitation
0.4
* *
0.2 0.0
*
-0.2 -0.4
0.4
Correlation coefficient
1995
Fig. 7. Pearson’s correlation coefficients between the stabilized frequency of double rings (f) using all discs and monthly climatic data. The broken lines shows the significance level at p < 0.05. *, p < 0.05; **, p < 0.01.
Correlation coefficient
0.0
1990
* *
0.2
*
*
* *
-0.6 -0.8
0.0
J
* **
-0.2
*
-0.4 -0.6 -0.8 O N D
J
F M A M J
Month
J
A S O N
wi sp su au
Season
the agreement between tree-ring width and dendrometer measurements confirmed that Q. ilex in the study area formed annual growth rings (Fig. 4). The periodical nature of tree rings can also be established by comparing the number of rings with the known age of the trees in plantations (Worbes 1995) or in trees that resprout after natural fires. In 2004, all trees were 21 years old, which means that the coppice stand in the study area resprouted in 1983 after a fire of 1982 (Lloret et al. 2003). Our results confirmed that it is possible to cross-date series of tree-ring widths of Q. ilex growing in a Mediterranean climate. Sampling cross sections at different heights helped to cross-date the tree rings and to identify the double rings. In
F
M
A
M
J
J
A
S
O
N
D
Month
some cases, correct tree-ring identification was only possible by comparing the disc with its adjacent cross sections. The structures of the lower, middle, and upper section standard chronologies were similar after standardization. Chhin and Wang (2005) also found that sampling height did not affect the ability of Picea glauca (Moench) Voss chronologies to detect climatic signals. Tree-ring width of Q. ilex was related to precipitation in spring and summer (Fig. 5). These results are consistent with a previous study of Q. ilex, which showed that radial growth was determined by the precipitation occurring in late spring–summer rather than by the mean annual rainfall (Cartan-Son et al. 1992). This confirms that cambial activity is controlled mainly by water availability during the growing season, which is the main limiting factor in the Mediterranean climate, especially in areas where the soils have a lower water-retention capacity. Several studies have shown positive correlations between tree-ring width and precipitation in the preceding autumn, as the water accumulated in the soils can be used during the next vegetative period #
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Fig. 8. Comparison of the cumulative relative radial growth (mean ± SE) measured by dendrometers (n = 10 trees) and daily precipitation (vertical bars) in 1995, 1996, and 1997. 150
1995
1996
1997
0.8 100 0.6
0.4 50 0.2
Daily precipitation (mm)
Relative radial growth
1.0
0.0 0 J
F M A M
J
J A
S O N
D
J
F M A M
J
J A
S O N
D
J
F M A M
J
J A
S O N
D
Month
(Cartan-Son et al. 1992; Corona et al. 1995; Nabais et al. 1998–1999). In our study, the lack of response to precipitation in the previous autumn could be attributed to the lower water-retention capacity of the soil. Quercus ilex showed a clear winter growth stop, as detected by the dendrometers (Fig. 8). In Italy, Q. ilex growing near Pisa showed an unclear winter growth stop, while in another area (Rapolano), at similar latitude but under continental influence, a clear winter stop was reported (Cherubini et al. 2003). In our study area, Q. ilex started to form wood in approximately April. Spring growth (April–June) was fast during the formation of early pores. Quercus ilex and other Mediterranean oaks have previously shown a strong radial increment in April and May (e.g., Zahner 1968; Nabais et al. 1998–1999; Garcı´a Gonza´lez and Eckstein 2003). In the present study, tree-ring width and precipitation in June and July were not significantly correlated. The lack of response to July precipitation could be explained by the lower amount of mean precipitation in this month (
