Trees (1998) 12: 187 ± 195

Ó Springer-Verlag 1998

O R I G I N A L A RT I C L E

Marco Borghetti ? Sergio Cinnirella ? Federico Magnani Antonio Saracino

Impact of long-term drought on xylem embolism and growth in Pinus halepensis Mill.

Received: 4 August 1997 / Accepted: 1 October 1997

AbstractmThe present study was carried out to elucidate the response mechanisms of 50-year-old Pinus halepensis Mill. trees to a long-term and severe drought. The amount of water available to trees was artificially restricted for 12 months by covering the soil with a plastic roof. Over the short term a direct and rapid impact of drought was evident on the water relations and gas exchanges of trees: as the soil dried out in the Spring, there was a concurrent decrease of predawn water potential; transpiration was strongly reduced by stomatal closure. Seasonal changes in the water volume fractions of twig and stem xylem were observed and interpreted as the result of cavitation and refilling in the xylem. When droughted trees recovered to a more favourable water status, refilling of embolized xylem was observed; twig predawn water potentials were still negative in the period when the embolism was reversed in the twig xylem. A few months after the removal of the covering, no differences in whole plant hydraulic resistance were observed between droughted and control trees. Needle and shoot elongation and stem radial growth were considerably reduced in droughted trees; no strategy of trees to allocate carbon preferentially to the stem conducting tissues was apparent throughout the experiment. An after-effect of the drought on growth was observed.

M. Borghetti ( ) ? A. Saracino Dipartimento di Produzione Vegetale, UniversitaÁ della Basilicata, Via N. Sauro 85, I-85100 Potenza, Italy Tel.: +39 971 474167; Fax: +39 971 474269; e-mail: [email protected] S. Cinnirella Istituto di Ecologia e Idrologia Forestale, CNR, Via A. Volta (Pal. Fabiano), I-87030 Castiglione Cosentino (CS), Italy F. Magnani1 Institute of Ecology and Resource Management, University of Edinburgh, Darwin Building, Mayfield Road, Edinburg EH9 3JU, Scotland, UK Present address: 1Istituto Miglioramento Genetico delle Piante Forestali, CNR, Via A. Vannucci 13, I-50134 Firenze, Italy

Key wordsmAleppo pine ? Climate change ? Water stress ? Cavitation ? Transpiration

Introduction

Water availability in Mediterranean regions is likely to be altered by the increase in atmospheric carbon dioxide and related climate changes. Predictions have been made that as CO2 supply to plants increases, their water supply may decrease (Parry 1992). Therefore, a proper understanding of the response mechanisms of trees to water shortage is a prerequisite for making predictions on the impact of climate change on the Mediterranean forests. Water availability affects trees in several ways and the whole plant response to drought is complex. Adjustments of stomatal conductance and carbon allocation are both considered as important response mechanisms to drought. The reduction of transpiration by stomatal closure should be considered as an `elastic' plant response, while the reduction of transpiration triggered by a change in allocation patterns (less carbon to the transpiring surfaces, more carbon to the conducting tissues) may lead to a `plastic' acclimation response. Combined low soil water contents and high vapour pressure deficits can induce xylem embolism, which is defined as the blockage of xylem conduits by air emboli due to xylem cavitation (Tyree and Sperry 1989). The vulnerability of xylem to cavitation is considered as an important factor determining the response of plants to water shortage. The hypothesis has been proposed that the vulnerability of xylem to water stress-induced embolism imposes a limit on resource allocation, and that conifer species tend to maximise long-term growth within the limits imposed by xylem embolism and related hydraulic constraints (Magnani et al. 1996). The present study was carried out to investigate the response mechanisms of Pinus halepensis Mill. trees to a severe and long-term drought. The amount of water available to trees was artificially restricted for 12 months and the

188 Table 1mSoil characteristics, upper 40 cm Sand (%) Silt (%) Clay (%) pH Organic matter (g kg±1 dw) Total N (g kg±1 dw)

Table 2mRainfall (mm) at the study site 95.9 0.6 3.5 7.9 11.0 0.7

impact on the water relations and growth was monitored. The hypothesis was tested that even under extreme drought no runaway xylem embolism ± sensu Tyree and Sperry (1988) ± and no irreversible xylem disfunction may occur, due to the control of transpiration by the adjustment of stomatal aperture or carbon allocation. Pinus halepensis is an important tree species of the Mediterranean basin (Nahal 1962).

Materials and methods Study area, experimental design, plant material The study was carried out in 1995 and 1996 in a natural Pinus halepensis Mill. forest growing at Castellaneta in the province of Taranto, southern Italy (40° 299 N, 16° 589 E, sea level). Soil in the experimental area is sandy, 42-m deep, showing a thin humic layer and a slight accumulation of organic matter in the upper 40 cm (Table 1); tree roots are concentrated in the upper 40 ± 60 cm of soil. The average annual temperature is 16°C and the annual rainfall 535 mm; a drought period normally occurs in the area between May and September (Table 2). An even-aged 50-year-old stand was selected, with the following characteristics: tree density 1856 ha±1; basal area 21.1 m2 ha±1; mean diameter at 1.3 m : 13 cm; tree height: 8 ± 10 m; leaf area index: 1.3. Six experimental plots (average surface >270 m2) were defined 50 ± 100 m apart from each other. Three plots were randomly assigned to the drought treatment and three were used as control plots. Leaf area index (LAI) was measured with a canopy analyser (LAI-2000, Li-Cor, Lincoln, Neb., USA): no significant difference was found between the average LAI of drought treatment and control plots at the beginning of the experiment. In the drought treatment, the water available to trees was restricted for 12 months (from December 1994 to December 1995) by suspending a `roof' made up by transparent polyethylene sheet at a height of 30 ± 50 cm above the soil. All plots were isolated from lateral water supply by a 2-m deep ditch. Environmental and physiological measurements Soil water content was measured throughout the experiment by time domain reflectometry (TDR) (Gray and Spies 1995). Two stainless steel cylindrical rods, 75 cm long and 5 mm in diameter, were fully driven into the soil 5 cm apart at three different places in each plot. A reflectometer (Soil Trase System 1, Soilmoisture Equipment, Santa Barbara, Calif.) was connected to the ends of the rods to determine the apparent dielectric constant of the soil (Ks). Ks was related to the soil water content by calibration against soil samples whose water content was measured gravimetrically while dehydrating in the laboratory. Plant water status was monitored by measuring the predawn water potential (Qp) of 1-year-old apical twigs by a Scholander pressure chamber. At each date, three twigs were sampled on each of 5 ± 7 trees per plot. The extent of embolism in the xylem of apical 1-year-old twigs and in the xylem of the main stem was estimated by measuring the volume fraction of water in the xylem (Vw). Three twigs per tree (the same

Month

53 years average

1995

January February March April May June July August September October November December

69 49 50 40 31 23 16 15 35 66 71 95

46 9 65 20 20 1 51 82 41 0.3 70 62

twigs used for the measurement of Qp), were sampled, and 2 ± 3 cmlong twig segments were detached, debarked and sealed with Parafilm. The volume fraction of water of debarked twig segments was determined as Vw = (Wf ± Wd)/(rw Vf), where Wf and Wd are the fresh and dry weight of segments, Vf is their fresh volume, determined as immersed weight in distilled water according to the Archimede's principle, and rw is the density of water; weights were measured to the nearest 0.1 mg and dry weight was determined after 48 h in an oven at 80°C (see Borghetti et al. 1991). The vulnerability of xylem to embolism was assessed by concurrent measurements of the volume fraction of water in the xylem (Vw) and water potential (Qt), made on a series of three detached 1-year-old apical twigs. Twigs were recut under water and allowed to rehydrate in degassed distilled water. While dehydrating on the bench, Qt was measured with the pressure chamber and Vw was assessed on 2 ± 3 cmlong twig segments, as described above. The water volume fraction of the trunk xylem was calculated from the dielectric constant of the xylem (Kx), which was measured by TDR. Two stainless steel cylindrical rods, 5 cm long and 3 mm in diameter, were fully inserted into the stem, 5 cm apart each other, at the height of 1.3 m on five trees per plot; the outer portion of the bark was removed in the area where the rods were driven into the stem and the exposed surface was coated with vaseline to prevent water loss from the xylem. Kx was related to the xylem water content by calibration against 10 ´ 10 ´ 7 cm xylem blocks whose water content was measured gravimetrically while dehydrating on the laboratory bench. At different dates throughout the year, daily courses of twig water potential (Qt), leaf conductance to water vapour (g) and sap flow (Q) were measured on 3 to 6 trees per treatment. Twig water potential was measured on three 1-year-old apical twigs per tree with the Scholander pressure chamber. Leaf conductance (g) was measured with a steady-state porometer (LI-1600, Li-Cor) on apical fully illuminated 1-year-old twigs; g was referred to the projected area of needles, which was measured with a LI-3000 area meter (Li-Cor). In Spring 1995, sap flow was measured by the thermoelectric `heat pulse' method, with a custom heat pulse velocity recorder (Soil Conservation Centre, Palmerston North, New Zealand). On each of three trees per treatment, four heating probes were inserted to different depths in the sapwood, at right angles to the surface and 1.30 m above the ground. Heat pulse velocity was measured every 30 min; sap flow was derived by the compensation technique (Huber and Schmidt 1937; Marshall 1958). Swanson and Whitfield's (1974) analysis was applied to correct for inhomogeneities caused by probe implantation wounds, which could affect the accuracy of the results; wound size was assumed to exceed by 5% the diameter of the drill (Dye and Olbrich 1993). Since autumn 1995, sap flow was also measured by the Granier's continuous heating method (Granier 1985, 1987) on three to six trees per treatment. Two probes (2 cm long and 2 mm in diameter) were inserted into the xylem at the base of the live crown, at a distance of 10 cm; probes were vertically aligned. The upper probe was continuously heated, whereas the lower one served as reference. The temperature difference between the probes was monitored every 15 min using a solid-state data logger (CR10, Campbell Scientific, Utah, USA), and

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Fig. 1mSeasonal variations of soil water content (Qs, upper graph) and predawn twig water potential (Qp, lower graph) in control (open circles) and covered (filled circles) plots. The vertical dotted line indicates the day when the plastic covering was removed. Vertical bars denote standard errors; differences between means were evaluated using the analysis of variance and the Duncan's multiple range test (P 50.05) related to sap flow using the equations proposed by Granier (1985). Sap flow was expressed as volume of water per unit area of sapwood (at the reference height of 1.3 m) and unit of time; sapwood was easily recognisable on xylem cores extracted from the trees at the end of the experiment. The two methods gave comparable results (data not shown). Throughout the experiment, the following tree characteristics were measured: the stem circumference at 1.3 m on five trees per plot, using aluminium increment bands; the length of current-year apical shoots (three cone-bearing and three vegetative apical twigs were sampled from three trees per plot); the length of all the needles from one apical twig sampled from three trees per plot. All the measurements were performed with a digital vernier caliper to the nearest 0.01 mm. Circular litter traps (surface = 0.25 m2) were suspended at 2 ± 3 m above the soil at three, randomly sampled, points in each plot. Needles were collected approximately every 2 weeks, and their dry weight was measured to the nearest 0.1 g after 48 h in an oven at 60°C.

Results

Seasonal changes of soil and plant water status In both covered and control plots the soil water content (Q) decreased during Spring 1995, with significant lower values in covered plots (Fig. 1). Between June and August, Q did not change in control plots; the increase of Q in covered plots at the beginning of July (from 0.02 to 0.04 m3 m±3) was probably due to the infiltration of water through the

Fig. 2mDiurnal patterns of twig water potential during selected days in April and August, in control (open circles) and covered (filled circles) trees. Vertical bars denote standard errors

plastic roof during a thunderstorm. At the beginning of August, Q was 0.03 and 0.023 m3 m±3, in control and covered plots. In control plots Q increased up to 0.1 m3 m±3 at the beginning of September, due to unusually heavy rainfall during August, declining to 0.06 m3 m±3 at the end of November. In covered plots the increase of Q from 0.02 to 0.05 m3 m±3 between August and November might have been due to capillary rise from the water table. In March 1996, 3 months after the removal of the plastic covering, Q was 0.12 m3 m±3 in both treatments (Fig. 1). Water release curves generated for soil samples collected from the study area show a near linear variation of water potential between ±0.2 and ±1.6 MPa for changes of Q between 0.09 and 0.05 m3 m±3. The seasonal trend of predawn twig water potential in control and covered plots (Fig. 1) agrees with the seasonal variation of Q. Since February 1995, predawn water potential of trees in covered plots (yp/cov) was lower than ±1 MPa and fell to a minimum of ±2.7 MPa on July 28. In the same period natural drought affected the water status of control trees; their predawn water potential (yp/unc) decreased from ±0.6 MPa at the beginning of April to ±2.5 MPa at the end of July; nonetheless, yp/cov was significantly higher than yp/unc throughout this period. yp/unc recovered to ±1 MPa at the beginning of September and did not show significant variations until the end of the experiment. On the contrary

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Fig. 3mMaximum daily values of leaf conductance (gmax) as a function of predawn water potential; gmax is expressed as a fraction of the maximum observed value in the period

Fig. 4mSeasonal variations of water volume fraction in the twig (upper graph) and in the stem xylem (lower graph), in control (open circles) and covered (filled circles) trees. The vertical dotted line indicates the time when the plastic covering was removed. Vertical bars denote standard errors; differences between means were evaluated using the analysis of variance and the Duncan's multiple range test (P 50.05)

yp/cov remained lower than ±1.5 MPa until the end of November. After the removal of the plastic covering, yp/cov recovered and no difference was observed between covered and control trees on 7 March 1996 (Fig. 1). The water stress integral (WSI), calculated for the whole period according to Myers (1988), was ±533 and ±813 MPa day±1 for control and covered trees, respectively. Twig water potential and leaf conductance Diurnal patterns of twig water potential (yt) were different in control and covered trees at different dates of the year (Fig. 2). Control trees showed common yt diurnal fluctuations (morning decline and afternoon recovery phase) at the beginning of April, when the predawn water potential

Fig. 5mWater volume fractions (Vw, dimensionless) in the twig xylem as a function of twig water potential (yt, MPa) (Vw = 0.64+0.034 yt, r = 0.58); 95% confidence intervals are reported

(yp/unc) was about ±0.6 MPa and at the end of August when yp/unc recovered to ±0.8 MPa; on June 10, when yp/unc was less than ±2.3 MPa, yt showed a slight decreasing trend for most of the day, and a weak recovery in late afternoon. A decreasing diurnal trend of yt was displayed by covered trees on April 19, when yp/cov was about ±2.0 MPa, whereas yt did not show substantial fluctuations on August 25; on March 7, the predawn water potential of previously covered trees recovered to ±0.9 MPa and common yt diurnal fluctuations, with morning decline and afternoon recovery, were observed (data not shown). Twig water potential never declined below ±3 MPa, despite a predawn water potential (ypd) to ±2.8 MPa. This was brought about by a sharp decrease of leaf conductance (g) to progressive drought, with a threshold of ypd for the onset of stomatal closure between ±1 and ±1.5 MPa (Fig. 3). Stomatal closure appeared in the covered plots first, in agreement with the earlier decline in soil water content and predawn water potential. As soon as a more favourable soil water content was restored in the Autumn, when ypd increased to ±0.8 MPa, stomatal functionality and transpiration recovered (see next paragraph).

Xylem embolism, transpiration and plant hydraulic resistance The water volume fractions in the twig xylem of control (Vt/unc) and covered (Vt/cov) trees were 0.69 and 0.66 on February 21; they both decreased over the Spring, falling to 0.54 and 0.56 on July 10; in most cases no significant difference was observed between Vt/unc and Vt/cov in this period. Vt/unc went up to 0.65 at the end of July and fluctuated between 0.6 and 0.65 until December. Vt/cov increased up to 0.61 at the end of July; afterwards a decreasing phase, with values down to 0.51 in October, was observed; over this period Vt/cov and Vt/unc differed significantly. In Spring 1996 both Vt/cov and Vt/unc recovered to 0.65 ± 0.7 (Fig. 4).

191 Fig. 6mDaily fluctuations of sap flow rates (measured with the Granier's continuous heating method, see text) in control (open circles) and covered (filled circles) trees, during Autumn 1995. Symbols represent the mean of six trees per treatment

Fig. 7mRelationships between twig xylem water potential (Qt, MPa) and sap flow rates (Q, g m±2 s±1) in Spring 1995 and 1996, in control (open circles) and covered (filled circles) trees. Regression equations are: yt = ±0.95 ± 0.05 Q, r = ± 0.78 (controls, 1995); yt = ±0.77 ± 0.05 Q, r = ± 0.71 (controls, 1996); yt = ±1.13 ± 0.02 Q, r = ± 0.66 (previously-covered trees, 1996). In Spring 1995 sap flow was measured with the `heat pulse' method; in Spring 1996 data gathered with both methods (the `heat pulse' and the `continuous heating' method) were pooled together

The water volume fractions in the stem xylem of control (Vs/unc) and covered (Vs/cov) trees were 0.53 and 0.56 on February 24. They decreased in early Spring: on April 27 the reduction was about 10% in both control and covered trees. Afterwards both Vs/unc and Vs/cov recovered, fluctuating between 0.5 and 0.55 for the rest of the time; throughout the whole experiment no significant difference was observed between Vs/unc and Vs/cov (Fig. 4).

A negative linear relationship was found between twig water potential and the water volume fractions in the twig xylem (Fig. 5). In Spring 1995, sap flow rates up to 18 ± 19 cm3 m±2 s±1 were measured in control trees (ypd >±1 MPa); on the other hand, in covered trees (ypd #±1.5 MPa) no values higher than 5 cm3 m±2 s±1 were found. When, at the end of November, ypd was higher than ±1.5 MPa, stomata opened

192

Fig. 10mNeedle fall during 1995 in control (open circles) and covered (filled circles) plots. Vertical bars denote standard errors; differences between means were evaluated using the analysis of variance and the Duncan's multiple range test (P 50.05)

Fig. 8mElongation pattern of shoots in control (open circles) and covered (filled circles) trees. The vertical dotted line indicates the time when the plastic covering was removed. Vertical bars denote standard errors; differences between means were evaluated using the analysis of variance and the Duncan's multiple range test (P 50.05)

Fig. 11mStem circumference increment during 1995 in control (open circles) and covered (filled circles) plots. Vertical bars denote standard errors; differences between means were evaluated using the analysis of variance and the Duncan's multiple range test (P 50.05)

regression line and the values of predawn water potential, which both give an estimate of the soil water potential, suggested that Q/yt relationships were interpretable according to the linear resistance model of water transport (Van Fig. 9mElongation pattern of needles in control (open circles) and den Honert 1948). When transpiration was heavily restrictcovered (filled circles) trees. Vertical bars denote standard errors; ed by stomatal closure and water potential gradients were differences between means were evaluated using the analysis of too low, as in covered trees in Spring 1995, hydraulic variance and the Duncan's multiple range test (P 50.05) resistance could not be estimated from Q/yt relationships. Hydraulic resistance did not change significantly after again and similar daily patterns and totals of transpiration 1 year in control plots and, in Spring 1996, the estimated R-values of control trees were even higher than those of were observed in control and covered trees (Fig. 6). An attempt to estimate temporal changes in the hydrau- previously-covered trees (Fig. 7). lic resistance (R) across the soil-plant continuum was made by plotting sap flow (Q) against twig water potential (yt) for selected days in Spring 1995 and 1996 (Fig. 7). R has Growth and needlefall been estimated as the proportionality constant between water potential difference and sap flow, according to the The elongation of current (produced in 1995) vegetative linear regression model (i. e. R = Dyt/Q); the agreement and female (cone-bearing) shoots was clearly affected by between the values of the intercept on the y-axis of the drought. Overall, in December 1995 the length of vegeta-

193

tive apical shoots and of female shoots showed a reduction of 30% (22 vs 31 mm) and 32% (70 vs 102 mm) in the drought treatment. In both treatments the rate of shoot elongation did not vary markedly throughout the growing season, being lower for covered trees (Fig. 8). The elongation of current needles was also affected by drought (Fig. 9). Overall, the length of current needles at the end of the season showed a reduction of 45% (36.5 vs 66.7 mm) in the drought treatment. Needles were 7 mm long on May 29 and did not grow until the end of July in both treatments. Needle elongation took place mostly between August and September; a further elongation phase took place in the Autumn (Fig. 9). On 9 May 1996, the length of current (produced in 1996) vegetative and female apical shoots showed a reduction of 44% (14 vs 25 mm) and 39% (31 vs 51 mm) in previously-covered trees (Fig. 8). Needle fall during 1995 (Fig. 10) was mainly concentrated between June and August in both treatments, with a pronounced peak in July. It started earlier in covered plots but reached a higher summer peak in control plots; in several cases significantly higher values were observed in control plots throughout the Summer and the Autumn; the total amount of needles shed (per unit ground area) was greater in control plots (Fig. 10). Until the end of July, no differences were observed in stem growth between covered and control plots; between August and October a rather constant growth rate was observed in control trees, whereas no growth was measured in covered trees; overall, in the period April ± December, the normalised increment of stem circumference was 2.8+0.74 mm and ±0.09+0.3 mm, in control and covered plots (Fig. 11). Between May and June 1996, substantial growth was observed in control trees but not in previouslycovered trees.

Discussion

In experiments performed in the field under Mediterranean conditions, it is difficult to have well watered control trees. Indeed, as a consequence of the scarcity of rainfall during Spring 1995, drought affected the soil water content and the water relations of trees both on the control plots as well as on plots where the water available to plants was restricted. A differentiated plant water status was apparent over the Summer and the Autumn, when the soil of uncovered plots was rewatered by rainfall (Fig. 1). Central to this study was the hypothesis that the impact of a prolonged drought may consist in the reduction of plant hydraulic conductivity caused by xylem cavitation and that, in order to avoid the catastrophic xylem disfunction, trees may respond to drought by the adjustment of transpiration (Tyree and Sperry 1988). Experimental evidence is accumulating on the adjustment of maximum sap flux densities according to the vulnerability of xylem to embolism and changes in whole-tree hydraulic conductances (Alder et al. 1996; Cochard et al. 1996); for instance, Lu et al. (1996) observed, in Picea abies, that the control of transpiration by

stomatal regulation maintain the minimum daily water potential above the threshold for xylem cavitation. A rapid response to soil drying was evident in our experiment. As the soil dried out in the Spring, leading to a concurrent decrease of predawn water potential, transpiration was reduced by stomatal closure. A rather high threshold (between ±1.0 and ±1.5 MPa) of predawn water potential for stomatal closure was found (Fig. 3), in accordance with previous data on Aleppo pine (Scarascia Mugnozza 1980; Aussenac and Valette 1982; Melzack et al. 1985; Grundwald and Schiller 1988; Schiller and Cohen 1995; Tognetti et al. 1997). Under Mediterranean conditions, a prompt response of plants to drought is crucial in order to prevent severe tissue dehydration and foliage dieback (Tenhunen et al. 1987; Pereira and Chaves 1993). A feedforward response of plants to soil drying mediated by chemical signals generated in the roots and transported via the xylem sap is often suggested (Davies and Zhang 1991; Khalil and Grace 1993; Jackson et al. 1995). It has also been suggested that any change in soil water content can result in hydraulic signals, which in woody species may be sensed by guard cells much earlier than chemical messengers (Saliendra et al. 1995). Our data suggest a role of stomatal closure in limiting the occurrence of cavitation. On the other hand, the relationship between water potential and the water content of the twig xylem (Fig. 5) does not suggest a critical threshold of water potential for the onset of xylem embolism. Therefore, the abrupt stomatal closure observed at a water potential of ±1.5 MPa may not be specifically related to hydraulic constraints in order to avoid excessive xylem cavitation and cycles of runaway embolism. Main evidences concerning changes in the water content of twig and trunk xylem were: the main decline was observed in Spring, in both control and covered trees; recovery phases were apparent in both control and covered trees, in the twig and trunk xylem; significant differences between control and covered trees were observed only for the twig xylem over the Summer and the Autumn; a few months after the removal of the covering, no differences were observed between control and previously-covered trees (Fig. 4). In conifers changes of the water volume in the xylem can be interpreted as the result of cavitation and refilling in the tracheids (Borghetti et al. 1991; Grace 1993), potentially affecting plant hydraulic resistance. For some reasons, however, the quantitative interpretation of how much these changes might have altered whole-plant resistance is not straightforward in our experiment. As previously pointed out, it was not possible to estimate whole-plant hydraulic resistance from Q/yt relationships in the Spring, when main changes in the xylem water content were observed and cavitation was supposed to be occurring. Embolism might have occurred in the root xylem, which is considered more vulnerable to cavitation (Lo Gullo and Salleo 1993). In the case of the trunk xylem, changes in the water content may reflect the gas content of the older tracheids, which are less important in water conduction, or tracheids in the heartwood, which do not conduct at all.

194

Refilling of embolized xylem was observed at different times during the experiment, in accordance with previous observations on conifer trees in the field (Waring and Running 1978; Borghetti and Vendramin 1987). Predawn water potentials were still negative (about ±1 MPa) in the period when embolism was reversed in the xylem, and substantial refilling took place when no growth was apparent in apical twigs of previously-covered trees (Figs. 4, 8). Interpretation is difficult on how refilling may occur under these biophysical conditions (Borghetti et al. 1991; Edwards et al. 1994; Lewis et al. 1994). In hardwood species the reversal of xylem embolism is commonly associated with above or near atmospheric pressures in the xylem (Hacke and Sauter 1995) or the production of new xylem (Magnani and Borghetti 1995). The capacity to refill may be crucial in determining the recovery of tree species following drought stress (Grace 1993). If reversible, xylem embolism may be, at least partially, useful: the cavitation of a proportion of vessels may cause a localised release of tension in the surrounding xylem (Dixon et al. 1984) and `sources' of water at high water potential may become available; Schiller and Cohen (1995) showed that Aleppo pine trees can use internally stored water when soil water is scarce. Leading to the increase of whole plant hydraulic resistance, xylem embolism may also contribute to limit water use as soil water is exhausted. Overall, no runaway cavitation and irreversible reduction of water transport efficiency occurred as a consequence of drought in this experiment: uncovered trees recovered a favourable water status in August, previously covered trees few months after the plastic roof was removed; whole-plant hydraulic resistance did not differ before and after drought in control trees and, few months after the removal of covering, Q/yt relationships evidenced an even lower hydraulic resistance in previously-covered trees; no symptoms of heavy xylem disfunction were observed in terms of increased leaf shedding in droughted plot. Carbon allocation and growth patterns can be affected by drought in conifers (see Gower et al. 1995). Mencuccini and Grace (1995) found, in Pinus sylvestris, that the leaf to sapwood area ratio is influenced by site differences in air humidity; Berninger et al. (1995) observed that the architecture of Scots pine trees do acclimate to the site conditions, providing more carbon to the conducting xylem as the climate becomes drier; the proportion of needle mass to total above-ground mass was found to decrease with decreasing moisture status in Abies lasiocarpa (Kuuluvainen et al. 1996). The short-term impact of drought can be recognised in a tree species characterised by an indeterminate free growth, as with Pinus halepensis (Messeri 1948, 1953; Calamassi et al. 1988). In control trees the main growth phase was observed during August and September 1995, when a concurrent increase of predawn water potential was measured. The small but measurable stem circumference growth in covered trees between days 300 and 350 was associated with the increase of their predawn water potential above ±1.5 MPa. Leaf area was affected, in terms of needles and shoot elongation, by the imposed drought; cone

bearing shoots appeared to be affected to a lesser extent, allowing speculation on the adaptive advantage of reproductive organs under stress conditions (Kozlowski et al. 1991). It is worth noting that needle elongation was observed in covered trees during August, when their predawn water potential was below ±2.0 MPa and stomata supposed to be closed. Stomatal conductance and assimilation rate may be affected differently by soil water potential; in a study on the response of Douglas fir seedlings to soil drying, Fuchs and Livingston (1996) found that stomatal conductance declined earlier than photosynthesis in response to the decline of soil water content. The resulting increase of water use efficiency at low soil water content could be interpreted as an adaptation to drought-prone environments. Overall, the percentage reduction of twigs and needle elongation, and stem growth (on an area basis) was 30 ± 32, 45 and 90%, respectively Therefore, a strategy of trees to allocate carbohydrates preferentially to the stem conducting tissues was not apparent in our experiment. In 1996, stem growth was considerably reduced in previously covered trees, suggesting a pronounced after-effect of drought on the current year cambial activity, which in tree species is based to a great extent on the translocation of previously stored carbohydrates (Dickson 1989). The hypothesis that severe drought may interact with other stress factors, leading to prolonged effects and tree decline, may be considered; in a recent experiment Welburn et al. (1996) found that the interactive effect of drought and ozone reduce the levels of proteins, phenols and antioxidant compounds in Aleppo pines; the resulting increased susceptibility to photoinhibition may cause long-term effects on growth, and could be claimed as a reason for the decline of this species in some Mediterranean areas. AcknowledgementsmResearch supported by a EU-ENVIRONMENT grant (LTEEF project: Long-term effects of CO2 increase and climate change on the European forests). The technical assistance of A. La Polla and F. Mattia is gratefully acknowledged. We would like to thank the Corpo Forestale dello Stato (Gestione ex Azienda Demaniale delle Foreste, Ufficio di Martina Franca) for the permission to work in the forest.

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