IAWA Journal, Vol. 25 (2), 2004: 185–204

EFFECTS OF A SEVERE DROUGHT ON GROWTH AND ANATOMICAL PROPERTIES OF QUERCUS FAGINEA

Leyre Corcuera1, Jesús Julio Camarero1,2 & Eustaquio Gil-Pelegrín1,*

SUMMARY We studied the growth response to drought of a Quercus faginea Lam. stand in a xeric site in NE Spain, that experienced an intense defolia- tion in 1993–94. This event coincided with very low precipitation from November to February, the period when total monthly precipitation ex- ceeds evapotranspiration. We evaluated the effects of November–Febru- ary precipitation (recharge precipitation, RP) on internode length, radial growth, and wood anatomy. Quercus faginea showed reduced longitudi- nal and radial growth during the years with low RP, and most sampled did not produce latewood in 1993–94 but showed wide earlywood vessels. We observed the reverse for years with a high RP. Radial growth was enhanced by increased precipitation during January and May of the growth year. If severe droughts become more frequent, due to a greater climatic variability, extensive dieback of marginal Q. faginea popula- tions may be expected. Key words: Dendroecology, Mediterranean climate, , predicted hy- draulic conductance, xylem.

INTRODUCTION

Reduced radial growth has been frequently described in temperate and Mediterranean oak forests in Europe and North America (Delatour 1983; Tainter et al. 1983). The main causes pointed out to explain this are: pathogens, excessive competition among neigh- bouring trees, aging and increased susceptibility, air pollution, and climatic stress (Manion 1981). The climate can act as a predisposing factor to pathogens or as a direct cause of growth reduction (Hepting 1963; Tuset et al. 1996). In fact, droughts have been involved in the onset of reduction in oak growth (Tryon & True 1958; Becker & Lévy 1982; Tainter et al. 1990; Jenkins & Pallardy 1995), especially in xeric sites (Lévy et al. 1992). Water stress has also proved to be a predisposing factor to pathogen attacks on Mediterranean (Vannini & Scarascia 1991). In Mediterranean areas, summer drought and winter cold are the main factors limiting growth (Mitrakos 1980). Both factors also affect the xylem structure (Fritts 1976;

1) Unidad de Recursos Forestales, Centro de Investigación y Tecnologia Agroalimentaria, Go- bierno de Aragón, Apdo. 727, 50080 Zaragoza, Spain. 2) Departament dʼEcologia, Facultat de Biologia, Universitat de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Spain. *) Corresponding author: Dr. E. Gil-Pelegrin1 [E-mail: [email protected]].

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Schweingruber 1993, 1996). For instance, a decrease in the mean diameter of the conduits (tracheids, vessels) has been associated with a reduction of water availability in the soil (Carlquist 1975, 1977; Baas et al. 1983; Baas & Schweingruber 1987; Von Wilpert 1991; Zhang et al. 1992). However, winter precipitation is the likely underlying climatic factor in Mediterranean areas, because of its effect on soil water availability for subsequent growth in the spring. The vulnerability of xylem to cavitation and embolism is one of the main factors determining the drought tolerance of (Tyree & Sperry 1989; Cochard & Tyree 1990; Tyree & Ewers 1991; Tognetti et al. 1998). The theoretical hydraulic conductivity through xylem depends on the number of conduits and on their diameter. According to the Hagen-Poisseuille law, the hydraulic conductivity of a cylindrical conduit is proportional to its diameter raised to the fourth power (Tyree et al. 1994). Consequently, the wider vessels are more effective hydraulic conduits, but entail a greater risk of drought/frost-induced embolism (Sperry & Sullivan 1992; LoGullo et al. 1995; Sperry et al. 1994; Tyree et al. 1994). According to the Intergovernmental Panel on Climate Change (IPCC 2001), a decrease in precipitation, a rise of mean temperature (2–4 °C), and an increase both in the frequency and intensity of acute droughts are expected for the (Houghton & Yihui 2001). Indeed, a 20% reduction in the total precipitation and an increased frequency of anticyclones have been observed in the Central-Western Mediterranean Basin between 1951 and 1995 (Piervitali et al. 1997). In the Iberian Peninsula, the 1980–95 period was characterized by intense droughts, which affected several woody (Font Tullot 1988). In the stand under study, a yellowing of followed by an intense defoliation was observed in 1993–94, affecting both Quercus ilex subsp. ballota (Desf.) Samp. and Quercus faginea Lam. (Aït-Bachir 1998). While Q. ilex subsp. ballota appears in continental areas in N and the Iberian Peninsula, Q. faginea is dominant in sub-Mediterranean forests in NE Spain between 600 and 1200 m a.s.l. (Blanco et al. 1997). Quercus faginea is a oak which forms ring-porous wood. It is usually found in sites with basic soils and summer precipitation greater than 100 mm (Ceballos & Ruiz de la Torre 1979; Jiménez et al. 1998). However, the most affected Q. faginea stands showed again a good vigour in 1996. This episode of intense defoliation in 1993–94 was also observed in other areas in NE Spain (Lloret & Siscart 1995). Hence, our main objective was to determine how the radial growth of Q. faginea responded to the intense 1993–94 drought. Specifically, we evaluated the relationship between low recharge precipitation (hereafter, RP) and growth reduction. We computed RP as the accumulated monthly precipitation from November prior to the growth year to February of the growth year, i.e. winter precipitation. This period was selected because: 1) during the RP months the total monthly precipitation is higher than the monthly evapotranspiration, which determines soil water availability for subsequent spring growth (Faci González & Martínez Cob 1991), and 2) radial increment is great in the Mediterreanean oaks during April–May (e.g., Zahner 1968). We focused on the growth and the xylem structure through a detailed study of the anatomy (number and diameter of vessels, vessel density) since these features were shown to be sensitive to the yearly variations in precipitation in other ring-porous

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oaks such as Q. macrocarpa (Woodcock 1989a). Pure or mixed oak coppice stands (especially Q. ilex subsp. ballota, Q. pyrenaica Willd., and Q. faginea), characterized by a long history of intensive human use for fuel-wood and charcoal production, are very abundant in the Iberian Peninsula (Serrada et al. 1992). Due to the abandonment of their traditional management, the customary cutting frequency decreased in the 1940s (Cañellas et al. 1996). Nowadays, most of the stems are over-aged (30–50 yrs.), which might make them more sensitive to climatic disturbances such as severe droughts because of their lower hydraulic efficiency (Amorini et al. 1996). In addition, the over- aged coppice stands of Mediterranean oaks form a new landscape that is still poorly studied from an ecological point of view (Enjalbal et al. 1996).

MATERIALS AND METHODS Study site A coppice stand dominated by Quercus faginea and Q. ilex subsp. ballota was selected in the Sierra de Santa Cruz-Cubel, Zaragoza, NE Spain (1° 39' W, 41° 07' N, 1177 m a.s.l.). The precipitation and temperature data were obtained from the Cubel-Casas Altas station located at c. 2 km from the stand (41° 06' N, 1° 38' W, 1108 m a.s.l.; period 1969–97). We also used precipitation data from the nearby Daroca station (41° 07' N, 1° 25' W, 779 m) to describe the temporal evolution of the rainfall in the area during the 20th century (1910–99 data). In the study area, the dry period in summer lasts c. 2 months, from the end of June to early September (Fig. 1). Since 1960, the following periods showed very low RP records: 1973–75, 1981–84, 1989, and 1992–95 (Fig. 1 & 2). In fact, the two lowest values for the total precipitation in January in the last 50 years in the study area were recorded in 1983 and 1993, respectively. The climate of the study area shows a transition from sub-Mediterranean to Medi- terranean (Allué Andrade 1990). The landscape was previously dominated by coppice stands of Q. faginea, but Q. ilex subsp. ballota is currently the most abundant species due to selective logging. Intense coppice management for fuelwood was carried out 40–50 years ago. The study site is located on very poor soils developed over Tertiary limestone outcrops. We assume that the thin soil and the high elevation of the study site make the trees of both species very susceptible to climatic stress (high sensitivity).

Sampling procedures The sampling was done in January 1998. Ten stems were cut at mid-height (c. 1.3 m) from the S-SW side of ten dominant multistemmed Q. faginea individuals (one stem per individual) for the analyses of wood anatomical variables (n = 10). Five additional stems were sampled from other individuals for the measurement of tree-ring width, including earlywood and latewood width, and internode length (n = 15). The stems had a similar diameter and age (mean age (± SE) = 27 ± 2 years). Although the sample size was close to the minimum required in standard dendroecological studies (Fritts 1976), the detailed analysis of wood anatomical features made this the largest sample size that could be studied. The middle of the older internodal segment of each stem was transversally sectioned with a sliding microtome (Anglia Scientific AS200, UK).

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Cubel-Casas Altas (1108 m) A 1969–1997 [29] 11.3 °C 481 mm 100

40 80

60 T (°C) T 20 40 (mm) P

20

0 0 J F M A M J J A S O N D

B Daroca Cubel-Casas Altas 250 800

200 600

150 400 100

200

50 Annual precipitation (mm) Recharge precipitation (mm) Recharge

0 0 1970 1975 1980 1985 1990 1995 Time (years)

Fig. 1. Climatic description of the study area. – A: Climate diagram of the Cubel-Casas Altas meteorological station. Precipitation information: dotted area, precipitation < 2 temperature (dry period); area with vertical lines, precipitation > 2 temperature (humid season). Temperature in- formation at bottom: lower black block, frost months (coldest month with the mean minimum temperature ≤ 0°C); lower stripped block, period with probable frost (absolute monthly minimum temperature ≤ 0°C and mean minimum temperature of the coldest month > 0°C); lower white block, frost-free months. – B: Annual (lines) and recharge (bars) precipitation for two near- by stations (Cubel-Casas Altas: in grey; Daroca: in black) during the 1970–98 period. RP is accumulated precipitation November–February.

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5 A

4 dry years

/

3

2

1

0

1910-19 1920-29 1930-39 1940-49 4 B 1950-59 1960-69 1970-79 1980-89 3 1990-99

2 wet period (years) Frequency of wet

/

1 Longest dry

0

1910-19 1920-29 Time (decades) 1930-39 Fig. 2. Interdecadal variability in the study 1940-49 area according to the recharge-precipitation data from the Daroca meteorological station (1910–99 period). 1950-59 We have expressed two different components of the precipitation regime. – A : Frequency of wet 1960-69 (white box) and dry (black box) years per decade. – B: Length of periods with consecutive dry years. 1970-79 The dry and wet years are defined as those years with recharge precipitation lower or greater than the 1980-89 1910–99 mean ± 1 SD. 1990-99

Sections with a thickness of 15–30 μm were stained with safranin and fast green, de- hydrated through 96% ethanol, and permanently mounted on slides with Canada balsam. The stem cross sections were studied with a microscope (Olympus BH-2) equipped with a photo-microadapter (Olympus OM-Mount) and a camera (Olympus OM101) for slide printing. The photos were digitized and calibrated to measure the xylem parameters. All samples were visually cross-dated (Stokes & Smiley 1968).

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Table 1. Descriptive statistics of the growth and the wood anatomical variables for the 1980–97 mean series (n = 10–15 trees). — Abbreviations of the statistics: SD, standard deviation; τ (%), relative frequency (in percentage) of individual series showing a significant P( ≤ 0.05) time trend based on Kendallʼs tau (τ) coefficient; AR1, first-order autocorrelation; msx, mean sensitivity. Abbreviations of the variables: INTl, internode length; TRw, tree-ring width; EWw, earlywood width; EWvD, earlywood vessel diameter; EWvd, earlywood vessel density; EWc, total early- wood conductivity; EWca, relative earlywood conductive area; LWw, latewood width; LWvD, latewood vessel diameter; LWvd, latewood vessel density; LWc, total latewood conductivity; LWca, relative latewood conductive area.

Variables Mean ± SD Min. (year) Max. (year) τ (%) AR1 msx

INTl (mm) 30.79 ± 12.17 12.01 (92) 55.33 (80) 50 0.52 0.28 TRw (mm) 0.21 ± 0.05 0.11 (93, 94) 0.30 (80) 50 0.42 0.21 EWw (mm) 0.14 ± 0.02 0.10 (94) 0.16 (80, 96) 25 0.45 0.10 EWvD (μm) 68.68 ± 3.49 61.85 (86) 73.67 (94) 67 0.51 0.04 EWvd (mm-2) 90 ± 14 64 (92) 109 (81) 50 0.56 0.11 EWc (mm2) 1 18.93 ± 4.80 12.08 (83) 29.74 (97) 67 0.72 0.10 EWca (%) 46.03 ± 3.66 39.32 (80) 51.78 (88) 11 -0.05 0.09 LWw (mm) 0.07 ± 0.04 0.00 (93) 0.15 (82) 50 0.31 0.77 LWvD (μm) 13.48 ± 6.81 0.00 (93) 23.52 (82) 67 0.45 0.54 LWvd (mm-2) 84 ± 48 0 (93) 172 (89) 44 0.72 0.49 LWc (mm2) 1 0.16 ± 0.10 0 (93) 0.53 (81) 22 -0.01 0.63 LWca (%) 7.52 ± 4.21 0.00 (93) 16.64 (92) 33 -0.14 0.44 1mm4 × mm-2. Mean, minimum and maximum values must be multiplied by 10-4.

Wood-anatomical variables A sequence of 18 annual values was used (1980–97) because this was the period com- mon to all trees. In addition, the age-dependent variability of the diameter of the early- wood vessels was approximately stabilized for this cambial age (Huber 1993). The following variables were considered: longitudinal growth (shoot length), tree-ring width (mean of two radii per ring located at right angles), whole tree-ring area, mean vessel diameter, vessel density (number of vessels per transverse xylem area), and conductive area (transversal area occupied by vessels). The last five variables were measured sepa- rately for earlywood and latewood. The abrupt shift in vessel size across the ring allow- ed us to identify the two types of wood (earlywood and latewood). Vessel-related vari- ables (diameter, density, conductive area) were measured in a standard area formed by a rectangle, 5 mm wide, along the tangential axis. Firstly, as the tree-ring width and other variables followed a biological growth-trend due to the aging and the increase in size, we converted the raw data into indexed values for each series to maximize their climatic signal (Fritts 1976). Secondly, we obtained mean annual values for all the variables averaging the indexed values of different indi- viduals. Detrending was done fitting simple linear functions, performing a first-order autoregressive model (see Table 1) to obtain the residual series, and averaging the index- ed values to obtain a mean indexed series. The standardized indices were constant with

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respect to the mean and variance. These calculations were carried out using ARSTAN (Cook 1985; Cook & Holmes 1992). Predicted hydraulic conductance (Kh; mm4) was calculated, according to the Hagen- Poiseuille law, as the sum of the fourth power diameters of all the vessels from each section. Previous studies had only considered the 10–25 widest conduits per section as a good approximation to estimate the predicted hydraulic conductance (Woodcock 1989a; Villar-Salvador et al. 1997). In this study, we measured for each tree ring all the vessels with a diameter greater than 10 μm within the 5 mm wide rectangle. The smallest and largest diameters were averaged for all measured vessels. The temporal trends of several variables were assessed using Kendallʼs tau (τ) coef- ficient (Table 1).To describe the interannual variability for the measured variables, we used the mean sensitivity, which ranges from 0 to 2 (Douglass 1936). This measure is calculated as the average mean sensitivity for a series (msx): msx = (1 / (n-1)) ∑ | 2 (xt+1 – xt) / (xt+1 + xt) | [1] where: n is the number of observations, and xt+1 and xt are the consecutive annual values of the measured variable.

Climate-growth relationships The influence of monthly precipitation and mean temperature on the tree-ring width was analyzed by means of correlation and response function analyses between tree- ring indices and climate variables using PRECON ver. 5.17B (Fritts et al. 1991). We performed 1000 iterations to obtain the bootstrapped response function in order to test the significance of the regression coefficients (Guiot 1990). We also compared the tree- ring width and the 10-day precipitation data from the Cubel-Casas Altas station using Spearmanʼs rank correlation coefficient r( s, Sokal & Rohlf 1995). The analyzed temporal window included October of the year previous to growth (t-1) up to September of the year of growth (t). This period was chosen based on the study of Tessier et al. (1994), which used the same span for studying growth-climate relationships in Mediterranean deciduous oaks. Finally, a Principal Component Analysis (PCA) was performed using the correlation matrix to determine independent axes of variance among the variables. All statistical analyses were done using SPSS version 6.1.2 (SPSS inc. 1989–1995).

RESULTS

In the 20th century, the longest period (4 consecutive years) with a low recharge precipi- tation was recorded between 1992 and 1995 (Fig. 1B & 2B). In the 1950s, there were a similar number of dry recharge-precipitation years, but only two of them occurred con- secutively (Fig. 2A). During the years with a low recharge precipitation, Q. faginea experienced a reduction of internode length, tree-ring/latewood width, and earlywood/ latewood area (Table 1, Fig. 3A & B). During the 1992–94 period, the values of the late- wood area were below the 1980–97 average (Fig. 3B). In fact, most of the stems did not produce latewood in 1993–94, particularly in 1993 (Fig. 3C). Nevertheless, we ob- served for all variables a subsequent growth recovery after the drought.

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1 mm

60 A

40

20

0.3

0.2

Tree-ring width Internode length Tree-ring 0.1 1980 1983 1986 1989 1992 1995 1998

8 B 6 ) (mm) 2 4

2

0 1980 1983 1986 1989 1992 1995 1998

100

75 C

50

25 Latewood absence Early- and latewood area (%) (mm 0 1980 1983 1986 1989 1992 1995 1998 Time (years) Fig. 3. Components of the annual longitudinal and radial growth of Quercus faginea. – A: Inter- node length and tree ring width. – B: Area of earlywood (grey triangles) and latewood (black triangles). – C: Annual frequency of trees without latewood. The error bars are standard errors. The vertical line represents the 1993 drought. At the top is a typical transverse section showing the variation in wood production (the arrows correspond to 1980 and 1990).

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200

) A 2 - 150

100

50

0 1980 1983 1986 1989 1992 1995 1998

80 10 m) m) Vessel density (mm Vessel m)

B μ μ 40 70 30

20 60 10

50 0 1980 1983 1986 1989 1992 1995 1998

0.6 ) LW vessel diameter ( ) LW ) EW vessel diameter ( ) EW 2 2 3 C

0.4 2

0.2 1 LW conductive area (mm LW EW conductive area (mm EW 0 0.0 1980 1983 1986 1989 1992 1995 1998 Time (years) Fig. 4. Vessel density (A), vessel diameter (B), and (C) conductive area for earlywood (grey tri- angles) and latewood (facing black triangles). The horizontal lines are the mean values for the 1980–97 period for earlywood (grey) and latewood (black). The error bars are standard errors. The vertical line represents the 1993 drought.

The earlywood vessel density showed a slight increase in 1993 (Fig. 4A), but the total earlywood area and the conductive area declined in 1993–95 (Fig. 4C). The latewood conductive area reached minimum values in 1993–94 because both the latewood vessel density and the mean diameter were very low in these two years (Fig. 4). Conversely, the mean diameter of the earlywood vessels was high for the 1991–94 period. A similar reverse relationship between the diameter of the latewood and the earlywood vessels was

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40

35

30

25 ) 4 20 (mm

Kh 15

10

5

0 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 Time (years)

Fig. 5. Total predicted hydraulic conductance (Kh) of earlywood (grey triangles, mm4 ⋅ 10-4) and latewood (black triangles, mm4 ⋅ 10-5). The vertical line represents the 1993 drought. observed in 1983 (Fig. 4B). The predicted hydraulic conductance (Kh) of the latewood was almost zero in 1993–94 (Fig. 5). The hydraulic conductance of the earlywood show- ed a trend increasing with time until 1991, but then decreased substantially from 1992 to 1994, and recovered in 1996 (Fig. 5). Several latewood variables (width, vessel diameter and density, conductivity) showed the highest mean-sensitivity values (Table 1). More than half of the vessel diameter series showed significant P( ≤ 0.05) temporal trends for early- and latewood. The highest first-order autocorrelation coefficients were obtained for the earlywood conductivity and the latewood-vessel density. The mean diameter of the early- and latewood vessels stabilized when the stems reached ages of c. 15 and 5 years, respectively (Fig. 6). This age-trend was more pro- nounced for the diameter of the earlywood vessels than for that of the latewood vessels. The diameter distribution of the vessels was bimodal (Fig. 7). In dry years such as 1993, there was a greater proportion of wide earlywood vessels (diameter 80–160 μm), and a lower relative number of narrow latewood vessels (diameter 10–40 μm; Fig. 7). A re- verse effect was observed in the wet years such as 1997. The tree-ring width was highly and positively correlated with the latewood width and the mean diameter of the latewood vessels (Table 2). A significant positive but less pronounced relationship was also found between the ring width and the internode length. The first three axes in thePCA based on growth and wood anatomical variables accounted for 68.9% of the total variance. The PCA axes were characterized by the following variables (Table 3): 1) latewood vessel density and conductive properties (axis I), 2) ring/latewood width and earlywood vessel diameter (axis II), and 3) early- wood vessel density and conductive properties (axis III).

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160 A

140 m) μ

120

100

80 400 200 n 60 0 0 5 10 15 20 25 Age (years)

60 B

m) EW vessel diameter ( m) EW 50 μ

40

30 LW vessel diameter ( LW

20 800 n 400 10 0 0 5 10 15 20 25 Age (years)

Fig. 6. Changes in the mean vessel diameter with increasing age of Quercus faginea stems for (A) earlywood (EW) and (B) latewood (LW). The box plots indicate the median (horizontal central line), the mean (thick horizontal central line), the 25% and the 75% percentiles (box limits), the 5% and the 95% percentiles (error bars), and the outliers (black dots). The lines represent the sample size (n, number of measured vessels).

The analysis of the response of tree-ring width to monthly precipitation and mean temperature revealed a positive (r = 0.68) and highly significant P( < 0.01) relation between the RP and the tree-ring width index. The recharge precipitation, and par- ticularly that recorded in January of the year of growth (t), greatly affected the radial growth of Q. faginea (Fig. 8A). However, the precipitation registered in May (t) was

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25

1993 mean 20 1997

15

10 Frequency (%)

5

0 0 20 40 60 80 100 120 140 160 180 Vessel diameter (10-μm classes) Fig. 7. Relative frequency (percentage) of vessels by diameter for Quercus faginea. The vertical line separates earlywood (60–180 μm) from latewood (10–60 μm) vessels. We compare the mean frequency distribution (black bars) with those of two contrasting climatic years: 1993 (dry year, grey bars) and 1997 (wet year, white bars). Error bars are standard errors.

A 0.6 0.4

0.2

0.0

-0.2

-0.4

-0.6

t-1 t Time (months) B 0.4

0.2

0.0

-0.2 Regression coefficient Correlation

-0.4

t-1 t Time (months)

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the only significant climatic variable in the response function (Fig. 8B). Only July t( ) precipitation and mean temperature had clearly reverse correlations. When the 10-day precipitation data were used, we found significant P( ≤ 0.05) positive relationships between the ring-width index and the precipitation corresponding to early January (t) (rs = 0.63) and late May (t) (rs = 0.48).

DISCUSSION

In Quercus faginea, radial growth responded to changes in recharge precipitation. Our re- sults are in line with other studies such as that by Tessier et al. (1994), who showed a direct response of the Q. pubescens radial growth to the precipitation recharge in sites in S France with well-drained calcareous soils and water deficit. Castro-Díez and Montser- rat-Martí (1998) found that the phenological pattern of Q. faginea in NE Spain is similar to that of those species with deep roots able to use the predictable water supply, such as that derived through December–January precipitation. Higher precipitation in the months January and February was correlated with wider tree rings in studies of temperate oaks (Eckstein & Frisse 1982). Costa et al. (2001) identified a significant positive influ- ence of the cumulative precipitation in the previous autumn (October–November) on Q. suber radial growth. Other studies with deciduous Mediterranean oaks have found a dominant direct response of radial growth to spring (Amorini et al. 1996) and summer (Tessier et al. 1994) rainfall. Several studies have also reported a positive influence of the warmer springs and wetter summers during the growth year on the tree-ring width of Q. robur and Q.petraea in temperate forests in Britain (Pilcher & Gray 1982), Germany (Eckstein & Frisse 1982), Italy (Nola 1991), and N Spain (Pérez Antelo 1993; Rozas Ortiz 1999). Our finding of a positive effect of the prior October temperatures on the ring width (Fig. 8) could imply an elongation of the late growing season in autumn. A strategy of delayed shedding has already been suggested for other deciduous Mediterranean oaks (Abadía et al. 1996). Nevertheless, the possible elongation of the growing season should be examined in the future through long-term phenological studies. Eckstein and Frisse (1982) found a significant positive influence of the recharge precipitation and a negative influence of the spring temperatures of the year of growth on the vessel area for Q. robur in Central Europe. Contrastingly, Huber (1993) only detected a positive effect of the mean maximum temperature during the previous autumn (September–December) on the area of the earlywood vessels of Q. robur and

← Fig. 8. Correlation (A) and response function (B) analyses of Quercus faginea radial growth and monthly meteorological variables (total precipitation: black bars; mean temperature: white bars). Radial growth and climate were compared from October of the year previous to growth (t-1) through September of the year of growth (t). In the upper graph, the horizontal grey lines are significance thresholds, while the asterisk in the lower graph indicates significant regression coefficient P( ≤ 0.05). The corrected R2 of the stepwise multiple regression was 0.71. In the cor- relation analyses, no correlation coefficient is significant (P > αʼ) if a Bonferroni correction is applied (Legendre & Legendre 1998), where αʼ is the modified probability level (αʼ = α / n = 0.002), and α and n are the conventional probability level (α = 0.05) and the number of paired comparisons (n = 24), respectively.

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LWc LWc 0.83*** —

Quercus Quercus faginea 0.89*** — 0.88*** LWvd

0.57* — 0.71** 0.39 . LWvD LWvD P

≤

ʼ ʼ

α

= 66 are the number of paired comparisons) for comparisons) paired of number the are 66 = n 0.75*** — 0.13 0.34 LWw LWw -0.04

0.01; ***:

≤

P = 0.05 and 0.05 = 0.06 0.19 0.28 0.25

-0.11 — -0.11 EWca α < ʼ ʼ α

0.61** — 0.15 0.19 0.35 EWc -0.29 -0.04 0.05; **: ≤

P

= 10–15). The abbreviations are as in Table 1. Significance levels were computed computed were levels Significance 1. Table in as are abbreviations The 10–15). = = 0.00038, where 0.00038, = < n n 0.01 0.41 0.01 EWvd -0.47* — -0.38 -0.27 -0.28 / α

ʼ = ʼ

α

0.12 -0.27 — -0.17 -0.65** -0.56* -0.26 -0.38 -0.10 EWvD

0.01 0.54* 0.41 0.08 0.12 0.05 EWw -0.51* — -0.02 -0.42

, Spearmanʼs coefficient) between the growth and the wood-anatomical variables of s

r

TRw 0.63** — 0.36 0.98*** 0.74*** 0.13 0.31 -0.66** -0.25 -0.17 -0.06

0.47* — 0.38 0.50* 0.48* 0.12 INTl -0.54* -0.57* -0.24 -0.09 -0.09 -0.23

INTI — EWw EWvD EWvd EWc EWca LWw LWvD LWvd LWc LWca Variables TRw Table 2. Table Correlation values ( ( variable each for series average the 1980 using period –1997 ( probability Bonferroni-corrected a obtaining after multiple comparisons (Legendre & Legendre 1998): *: 0.01

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Table 3. Principal Component Analysis (PCA) of the growth and the wood-anatomical variables of Q. faginea for the 1980–1997 period. — The abbreviations are the same as in Table 1. The vari- ance explained by each axis is shown. The PCA was based on the correlation matrix using all the individual data (n = 180). The three variables with the highest scores in absolute values for each axis are in bold.

Variables Axis I (33.3%) Axis II (20.4%) Axis III (15.2%) INTl 0.35 0.33 -0.05 TRw 0.69 0.64 -0.10 EWw 0.43 0.34 -0.42 EWvD 0.02 -0.69 -0.13 EWvd -0.07 0.58 0.48 EWc 0.29 -0.32 0.75 EWca 0.40 -0.05 0.87 LWw 0.65 0.62 0.08 LWvD 0.86 -0.01 -0.17 LWvd 0.73 -0.36 -0.07 LWc 0.76 -0.43 -0.06 LWca 0.82 -0.43 -0.09

Q. petraea. The influence of the precipitation on the interannual variation of latewood vessel diameter is greater than on the ring-width changes in Q. macrocarpa (Woodcock 1989a). However, Villar-Salvador et al. (1997) did not find any significant relationship between the Q. faginea xylem features (mean maximum vessel diameter, vessel density, vessel element length) and the annual precipitation variability along a spatial gradient of aridity. Significant responses appeared when the species analyzed were evergreen oaks with diffuse-porous wood such as Q. ilex and Q. coccifera (Villar-Salvador et al. 1997). According to these authors, the lack of climate sensitivity of Q. faginea could be explained by the location of the stands studied in valley bottoms with abundant water reserves, which could have masked their sensitivity to the variations in precipitation. Location of our study site in an area prone to soil-moisture stress, regarded as a low- quality site for Q. faginea, could explain the reverse correlations between tree-ring width and temperature and precipitation for July (t), suggesting a negative effect of increased evapotranspiration on the radial growth (Fig. 8). For instance, Gasson (1985, 1987) and Sass and Eckstein (1995) showed that the precipitation deficiencies could have an immediate effect on the radial growth due to the low water-retaining capacity of the soil. In ring-porous wood, the variation in tree-ring width depends mainly on the amount of latewood produced (Tables 2 & 3; Woodcock 1989b, c). Based on our correlation analyses, longitudinal growth seems to be also integrated with wood formation. The high interannual variability of latewood variables (width, vessel diameter, and conduc- tivity) reflects the dominant climatic impact, particularly of the rainfall, on latewood development. This agrees with Pumijumnong and Park (1999), who found that the radial growth of teak, a tropical species with ring-porous wood, is influenced by the amount

Downloaded from Brill.com09/30/2021 01:25:47AM via free access 200 IAWA Journal, Vol. 25 (2), 2004 Corcuera, Camarero & Gil-Pelegrin — Drought effects in Quercus faginea 201 of rainfall during the transition period from the dry to the wet season. The earlywood features (width and vessel size) were much less variable (Table 1). Vessel diameter and vessel density were inversely correlated in the earlywood, but positively correlated in the latewood (Tables 2 & 3). This result is somewhat foreseeable since wide and closely spaced vessels are usually found in the earlywood (Woodcock 1989c). Interestingly, the diameter distribution of Q. faginea wood did not greatly deviate from bimodality (ring porosity) in contrasting climatic years. This conservative strategy may be related to the sub-Mediterranean distribution of Q. faginea, which emphasizes the role of recharge precipitation as a source of soil water reserves for spring growth in these transitional forests. The development of wide earlywood vessels allows ring- porous species to transport more water for their rapid leaf flush during the early growing season after the winter dormancy, but at the expense of an increased risk of embolism (Tyree et al. 1994). Since the earlywood vessels are derived from overwintering cells formed in the previous fall, the radial growth also responds to the variability of winter (January) and early spring (May) precipitation. The influence of the spring precipitation during the year of growth on the latewood formation can be explained by its greater metabolic cost due to a high non-conductive tissue content (Zimmermann 1983). The latewood can remain conductive for several years but accounts for less than 5% of the total flow through sapwood (Ellmore & Ewers 1986). In spite of the high values of earlywood vessel diameter and density (Fig. 4A, B) during the dry 1993–94 period (Fig. 1), the decrease in the earlywood area (Fig. 3) led to a reduction in the conductive area (Fig. 4C) and the total predicted hydraulic con- ductance (Fig. 5). During this period, most trees did not produce latewood, and these narrow rings were composed almost entirely of earlywood vessels. Therefore, the risk of cavitation increased greatly (LoGullo et al. 1995). Ponton et al. (2001) suggested that trees with a smaller earlywood vessel area might show greater water-use efficiencies. The reduction of the internode length during the drought period implies a lower leaf area (Corcuera, unpublished data) that might be considered a compensating mecha- nism to minimize the drought-stress injury (Adams 1994). The affected oaks recovered promptly and formed wide tree rings and long internodes with abundant foliage in 1996. Such short-term responses can be regarded as components of the phenotypic plasticity of the plants (Sultan 1995). Several climate assessments suggest a greater frequency and duration of severe droughts in Spain (IPCC 2001). Dendroclimatic reconstructions in the Iberian Peninsula have revealed an increased frequency of intense droughts during the second half of the 20th century (Manrique & Fernández-Cancio 2000). Rodó et al. (1997) reported for the study area a teleconnection between El Niño episodes in the Pacific Ocean and periods characterized by low recharge precipitation. Severe droughts were recorded in 1983 and 1994 after strong phases of the Southern Oscillation in 1982–83 and 1992–93. If the frequency of strong El Niño events increases in the future, it is expected that the radial growth of Q. faginea will be affected by frequent years with reduced recharge precipitation. Theoretically, if the severe droughts become more frequent and cause extensive dieback of these marginal Q. faginea populations, more drought-resistant trees such as Q. ilex would become dominant. Hence, the adverse effects of greater climatic variability should be considered for proper management of Q. faginea stands.

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CONCLUSIONS

We have shown how an over-aged Q. faginea coppice stand responded to an intense drought in 1993 by reducing the ring width, the internode length, and the predicted hy- draulic conductance. The radial growth decreased in response to a period of consecutive years (1992–95) with a low recharge precipitation, particularly January and February precipitation. The latewood width and vessel diameter were more sensitive to climatic variability than the earlywood features. There was a widespread latewood absence in the sampled trees during 1993–94, which led to a reduction in radial growth. Radial growth was enhanced by increased precipitation during January and May of the growth year.

ACKNOWLEDGEMENTS

This work was supported by 1FD97-0911-C03-01 project (Subpr. 1), an INIA grant to LC and an INIA-DGA postdoctoral contract to JJC. We thank several anonymous reviewers, and P. Baas and D. Woodcock for their valuable comments.

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