JXB Advance Access originally published online on July 28, 2003
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Journal of Experimental Botany, Vol. 54, No. 390, pp. 2015-2024,
September 1, 2003
© 2003 Oxford University Press
Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought
Received 17 October 2002; Accepted 22 May 2003
1 CEAM-Department de Ecologia, Universitat d’Alacant, POB 99, E-03080 Alacant, Spain
2 Department de Ecologia, Universitat d’Alacant, POB 99, E-03080 Alacant, Spain
3 CEAM, C/Ch. Darwin 14, Parque Tecnológico, E-46980 Paterna, Spain
4 Unidad de Recursos Forestales, SIA-DGA, POB 727, E-50080 Zaragoza, Spain
* To whom correspondence should be addressed. Fax: +34 965 903 464. E-mail: a.vilagrosa{at}ua.es
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Abstract |
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Seedling shrubs in the Mediterranean semi-arid climate are subjected to intense droughts during summer. Thus, seedlings often surpass their limits of tolerance to water stress, resulting in the loss of hydraulic conductivity due to xylem cavitation. The response in terms of stomatal conductance, vulnerability to cavitation, leaf dieback, and survival were analysed in two co-occurring seedlings of mastic tree (Pistacia lentiscus L.) and kermes oak (Quercus coccifera L.) during an intense drought period. Both species reacted to drought with steep decreases in stomatal conductance before the critical water potential brought about the onset of cavitation events. Q. coccifera showed wider safety margins for avoiding runaway embolism than P. lentiscus and these differences could be related to the particular drought strategy displayed by each species: water saver or water spender. The limits for survival, resprout capacity and leaf dieback were also analysed in terms of loss of conductivity. By contrast with previous studies, the species showing higher seedling survival in the presence of drought also showed higher susceptibility to cavitation and operated with a lower safety margin for cavitation. Both species showed a leaf specific conductivity (LSC) threshold below which leaf biomass had to be regulated to avoid runaway embolism. However, each species displayed a different type of response: P. lentiscus conserved total leaf area up to 100% loss of LSC, whereas Q. coccifera continuously adjusted leaf biomass throughout the drought period in order to maintain the LSC very close to the maximum values recorded without loss of conductivity. Both species maintained the capacity for survival until the loss of conductivity was very nearly 100%.
Key words: Drought stress, leaf dieback, Mediterranean shrubs, stomatal conductance, survival, xylem cavitation.
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Introduction |
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Soil water availability represents a major environmental constraint under Mediterranean conditions. Drought leads to water deficit in the leaf tissue, which affects many physiological processes and can have ultimate consequences for plant growth and survival. Among these processes, the loss of hydraulic conductivity in the xylem has been recognized as playing an important role in drought resistance (Tyree and Sperry, 1989). This phenomenon is due to xylem cavitation, i.e. breakage of the water column under negative xylem pressure (Zimmermann, 1983). Once a conduit cavitates and becomes air-filled (embolized), it is not available for water transport (Tyree and Sperry, 1989). Thus, cavitation reduces hydraulic conductivity in the xylem, and plants cannot supply their leaves with water properly.
Plants differ widely in their susceptibility to cavitation, and it has been suggested that a high cavitation resistance results in a higher tolerance to water deficit (Pockman and Sperry, 2000). Therefore, the survival of the species in climates with water limitations would be related to the resistance of their xylem to cavitate (Davis et al., 1998; Hacke et al., 2000). In this sense, it has been observed that vulnerability to embolism determines the patterns of survival in different species and that these patterns could affect species distribution (Pockman and Sperry, 2000). Moreover, after applying a survival model in Mediterranean species, Martínez-Vilalta (2001) reported that vulnerability to cavitation was the crucial variable for explaining differences in drought tolerance and survival.
In a Mediterranean context, global warming models predict generalized temperature increases as well as increases in the frequency of intense drought episodes and, in effect, both phenomena have already been observed (Piñol et al., 1998). Prolonged climatic changes could produce cavitation-induced species declines and, consequently, alterations in species composition at the community level (Tognetti et al., 1998). Therefore, differences in vulnerability to cavitation among species could have important implications for the survival of adult individuals, and these differences could be even more critical for the recruitment of young individuals that have less access to deep water reserves in the soil (Williams et al., 1997; Davis et al., 1998). In this sense, after analysing a wide range of Mediterranean species, Vallejo et al. (2000) found that seedling mortality during summer in the semi-arid Mediterranean (eastern Spain) increased with the length of the rainless period, and rainless periods longer than 120 d produced mortality rates above 80%. In fact, previous studies with Pistacia lentiscus and Quercus coccifera at the seedling stage showed steep decreases in water potential (i.e. less than –5 MPa) during a period of several months without rainfall in drought years, resulting in high mortality rates (Fonseca, 1999).
In addition, there is increasing evidence that xylem embolism limits gas exchange (Jones and Sutherland, 1991; Nardini and Salleo, 2000; Sperry et al., 2002), and can act as a control mechanism which, in connection with stomatal activity, regulates the amount of water extracted by the plant (Salleo et al., 2000; Cochard et al., 2002). It has generally been considered that species tend to operate near the point at which water potential causes catastrophic xylem dysfunction and that they must regulate transpiration to avoid the positive feedback that would increase the loss of hydraulic conductivity and runaway embolism (Sperry et al., 2002).
The principal aim of the present study was to investigate how seedlings of the co-occurring Mediterranean sclerophyllous shrubs, P. lentiscus L. (Anarcadiaceae) and Q. coccifera L. (Fagaceae), regulate water losses during an intense drought period in relation to the mechanisms for avoiding cavitation. A second objective was to attempt to ascertain the limits to survival in terms of loss of conductivity. Thus, changes in water potential, stomatal conductance, hydraulic conductivity parameters, leaf biomass, and survival capacity were monitored simultaneously.
Although both species are characteristic of the macchia on the Mediterranean arid range (Le Houérou, 1981), they show some interesting differences between them. Seedlings of P. lentiscus registered higher survival rates than those of Q. coccifera after plantation in reforestation programmes (Vilagrosa et al., 1997; Fonseca, 1999; Vilagrosa, 2002). Moreover, P. lentiscus is semi-ring-porous (Villar-Salvador, 2000), and it has been observed to follow a strategy of drought-avoidance by water-spending (Levitt, 1980; Vilagrosa, 2002). Q. coccifera, on the contrary, is diffuse-porous (Villar-Salvador, 2000), and shows a strategy of drought-avoidance by water-saving (Vilagrosa et al., 1997). Taking into account these differences, it was investigated whether stomatal conductance was limited by xylem cavitation in these species, what the safety margins were for avoiding the onset of cavitation events and what mechanisms were displayed to avoid runaway embolism after stomata closure.
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Materials and methods |
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Plant material
The local Forest Service supplied seeds of both species (from the Valencia, Spain, Regional Government seed bank) from the same area where the experiment was carried out (Mediterranean semi-arid climate, precipitation: 250–300 mm year–1 and average temperature: 17–19 °C). Two hundred 2-year-old seedlings for each species were grown in 8.0 l containers filled with forest soil under full sunlight conditions, and they were watered and fertilized as needed.
The drought period took place during summer in full sunlight at the SIA (Servicio de Investigaciones Agroalimentarias-DGA, Spain) experimental fields. Daily temperatures and relative humidity ranged between 20 and 37 °C and 40 and 80%, respectively. Photon flux density at midday was from 1700–2200 µmol m–2 s–1. Before the drought period began, the seedlings of both species were watered to field capacity and then allowed to dehydrate freely during the intense drought period.
Cell-water relationships
Pressure–volume (P–V curves) analysis was conducted in order to establish the critical point at which seedlings lost turgor. Since Mediterranean species have very short petioles, one leafy shoot with 5–6 leaves was selected to carry out P–V determinations. Five P–V curves were analysed in each species according to the methods of Tyree and Hammel (1972). From each curve, relative water content at turgor loss point (RWCtlp), water potential at the turgor loss point (
tlp), osmotic potential at full turgor (
o), and bulk modulus of elasticity (Emax) were estimated.
Stomatal conductance and water potential
Every three days throughout the drought period, five plants of each species were chosen randomly to measure stomatal conductance (gs) and predawn water potential (pd). A model LI-1600 Steady State Porometer (Li-Cor Inc., Lincoln, NE, USA) was used to measure stomatal conductance. For determination of maximal stomatal conductance (gs-max), measurements were taken at 3 h intervals throughout the day, from 06.00 to 18.00 h solar time. Measurements were made on the abaxial side of the leaves, and the sensor head of the porometer was held at the natural position and angle of the leaf during measurement. gs-max was related to pd according to Acherar and Rambal (1992), who established that pd determines the daily maximum values of gs (gs-max). Water potential in leafy shoots was assessed by means of a pressure chamber. To avoid tissue dehydration during measurements, the walls of the pressure chamber were covered with wet filter paper. Another set of plants (n=19 for P. lentiscus and n=15 for Q. coccifera) was used to establish the relationship between pd and midday water potential (md).
Leaf dieback, survival and resprout capacity
Leaf dieback was recorded in another set of plants that were subjected to the same intense drought period (n=22 and n=20 for P. lentiscus and Q. coccifera, respectively). Leaf dieback was computed as a percentage of reduction in leaf area as a function of water potential (xil). During the drought period, after seedlings attained a certain xil, they were rewatered to analyse survival and resprout capacity.
Vulnerability to embolism and hydraulic parameters
A total of n=20 and n=24 seedlings of P. lentiscus and Q. coccifera, respectively, were used to carry out the vulnerability curves. Vulnerability to embolism was measured in current-year twigs by constructing vulnerability curves through the dehydration method (Tyree and Sperry, 1989). For measuring xylem conductivity during the drought period, ten current-year twigs of one seedling were collected in which water potential (xil) had previously been measured. To avoid additional embolism the twigs were cut underwater in segments of 30–50 mm in length, and both ends were shaved with a razor blade. Since both species showed low relative growth rates, it was not possible to choose longer segments. However, preliminary determinations of maximum vessel length showed that the length of the longest vessel was very similar to the segment lengths chosen in this study. The segments were placed in a tubing manifold similar to the one described by Cochard et al. (1996). A more accurate description of the device can be found in Vilagrosa (2002). The manifold with the twigs was immersed in distilled water to prevent desiccation and to maintain a near constant temperature. The segments were perfused with a degassed HCl solution (0.5 ml l–1, pH
2) at low pressure (5.48 kPa) to measure initial hydraulic conductivity (Khi, kg m–1 s–1 MPa–1). The acid was used to minimize microbial growth in the tubing system and to avoid artefacts due to salt solutions used in previous studies (Alder et al., 1997; van Ieperen et al., 2000). Recent studies (Zwieniecki et al., 2001) found that acidic solutions could increase the flow throughout the stems after 40 min of flushing. In a previous study, several flushing times were tested (up to 20 min), finding no significant variations in the flow. However, to minimize possible artefacts, measurements were performed at short time intervals, about 15 min for the whole measurement in each segment.
Flow rate through the twig segment was measured gravimetrically with an analytical balance (Metlher AE 40) connected to a computer which calculated the flow rate of each twig segment. Hydraulic conductivity was calculated as the mass flow rate of the solution through the twig segment divided by the pressure gradient along the segment (Kh, kg m–1 s–1 MPa–1).
After the initial hydraulic conductivity (Khi) was measured, the twig segments were flushed with pressurized solution (100 kPa for 10 min) to remove any air emboli. It was verified that longer flushing times did not produce significant variations in the flow rates. Then, the same procedure as in Khi was followed to measure the maximum flow of water (Khmax). The percentage loss of conductivity (PLC) was computed as: (1–Khi)x100/Khmax. PLC was used to plot the reduction in cavitation-induced leaf specific conductivity (LSC) versus water potential (xil) as a new type of vulnerability curve. This type of vulnerability curve illustrated how large the reduction was in the capacity to supply water to leaves during the drought period. Modelled reductions (sigmoid regression) computed in drought-induced leaf dieback were used to correct the modelled decrements in LSC due to cavitation and then to calculate the real capacity of the xylem to supply water to leaves (LSCcorr). The same current-year twig segments were measured in length, diameter without bark, and leaf biomass supplied, to compute the main hydraulic architecture parameters: hydraulic conductivity (Kh), specific conductivity (Ks), and LSC.
Statistical analysis
All statistical analysis were performed by using SPSS version 10.0 package (SPSS Inc., Chicago, Illinois, USA). Data from P–V curves and hydraulic parameters were subjected to analysis of variance (one-way ANOVA) to detect differences between the species. Regression analysis was used to fit stomatal conductance, vulnerability to cavitation curves, LSC, and leaf dieback with water potential. Differences between species were tested with analysis of covariance since this technique combines regression analysis with ANOVA (Underwood, 1997). The lineal adjustment of the data was verified previously. The natural logarithm of water potential was the concomitant variable, and it was compared for the equality of slopes through the interaction of the concomitant variable and the factor. Data transformations were made when necessary to ensure the validity of the assumptions of normality, linearity and homoscedasticity.
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Results |
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Analysis of pressure–volume curves showed similar values for both species (P >0.05). Both species lost turgor between –3.3 to –3.5 MPa, and
o at full turgor was –2.6 MPa (Table 1). Emax values corresponded to relatively non-elastic cell walls, with high gradients of water potential associated with small losses in cell volume. RWCtlp remained relatively high for both species, with values ranging between 86 and 87% at the turgor loss point.
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Figure 1 shows the relationship between gs-max measured during the day and
pd. Generally, the gs-max was recorded during the early hours of the day. P. lentiscus showed higher rates of stomatal conductance with high water availability (491±99 mmol m–2 s–1) than Q. coccifera (173±15 mmol m–2 s–1). These values decreased suddenly when pd diminished only slightly (i.e. gs-max around 100 mmol m–2 s–1 at –1 MPa). After 24 d of intense drought, P. lentiscus showed lower gs-max values (26±12 mmol m–2 s–1), which corresponded to a pd of –4 MPa. Even with high water availability, Q. coccifera maintained conservative stomatal conductance rates which decreased more gradually with lower pd. The shape of the curves was significantly different between species (F1,15=7.84; P=0.01).
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According to gs-max results, P. lentiscus was more efficient in conducting water to leaves than Q. coccifera (P <0.01; Table 2). P. lentiscus exhibited much higher Kh than Q. coccifera, i.e. 29.8x10–7 and 5.0x10–7 kg m s–1 MPa–1, respectively. The differences between both species decreased when Kh was expressed as a function of sap-wood area (specific conductivity, Ks) or leaf area supplied (leaf specific conductivity, LSC). Nonetheless, the differences were still significant; P. lentiscus showed two times higher values than Q. coccifera for both parameters (P <0.01).
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In order to evaluate the reduction in the water supply to leaves as the plants got drier, the vulnerability to cavitation curves and the reduction in LSC due to cavitation as a function of
xil were analysed (Figs 2, 3). Both species were very resistant to cavitation events, but P. lentiscus was more susceptible to water stress-induced cavitation than Q. coccifera (F1,36=8.34, P <0.01) (Fig. 2). Cavitation events started at the critical water potential (crit) of –3.5 MPa for P. lentiscus, whereas loss of conductivity was close to 100% at –7.5 MPa. For Q. coccifera, crit was –5 MPa and all hydraulic conductivity was lost when xil was brought down below –10 MPa. As a consequence, P. lentiscus reduced LSC sooner than Q. coccifera and both curves crossed at –5.5 MPa (Fig. 3). At that point, both species showed the same LSC, about 1.1x10–4 kg m–1 s–1 MPa–1, but while P. lentiscus had lost 50% of LSC, Q. coccifera had lost only 20%. From this point, Q. coccifera continued losing LSC slightly until the xil decreased to –10 MPa. By contrast, P. lentiscus lost LSC completely in a short interval of xil, between –5.5 and –7.5 MPa.
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0) in both species. Number of samples was n=19 and n=21 for P. lentiscus and Q. coccifera, respectively.
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It is generally accepted that plants operate near the point at which
xil causes catastrophic xylem dysfunction (Pockman and Sperry, 2000; Sperry et al., 2002). The minimum water potential (midday water potential, md) as a function of predawn water potential (pd) was analysed in order to establish the responses to high water availability and intense drought stress in both species (Fig. 4). P. lentiscus showed a linear regression between pd and md, displaying a constant increment (md –pd about 1.6 MPa) independent of the pd values. This species operated near the critical water potential (crit), up to –2 MPa, at which point the md decreased under the crit and cavitation occurred. Q. coccifera showed an exponential regression indicating differential increases in md throughout the drought period. This species showed an increment (md–pd) of about 2 MPa with high water availability, which was progressively reduced (1 MPa at pd 
–4 MPa). Moreover, during the turgor phase, Q. coccifera operated very far from the point at which xil causes catastrophic xylem dysfunction.
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Leaf dieback and resprout capacity were also recorded during the drought period (Fig. 5; Table 3). Leaf dieback started when
xil was between –5 and –6 MPa and LSC was the same for both species (around 1.1x10–4 kg m–1 s–1 MPa–1). Afterwards, P. lentiscus lost all leaves in a short interval of xil (i.e. between –5 and –8 MPa). By contrast, leaf dieback was more progressive in Q. coccifera and this species lost all the leaves when xil reached values around –10 MPa. To clarify drought stress effects on loss of conductivity and resprout capacity, four phases were identified (Table 3). Phase 1 was characterized by a moderate loss of conductivity without visible damage on the plants. This phase continued until both species fell to –5 MPa and the loss of conductivity was 55 and 20% for P. lentiscus and Q. coccifera, respectively. During Phase 2, some leaf dieback occurred, but after rewatering, 100% of seedlings remained alive and no resprouts were observed. In this phase, xil remained between –5 and –7 MPa for both species. Loss of leaf area in P. lentiscus reached 50% when xil fell to –7 MPa and loss of conductivity was nearly 95%. For the same xil, loss of leaf area was only 30%, and loss of conductivity was 50% in Q. coccifera. Both species lost all leaves at the end of Phase 3. But, at rewatering, both species resprouted from the base of the shoots and all seedlings remained alive. This phase was very short for P. lentiscus (xil between –7 and almost –8 MPa), whereas for Q. coccifera it ranged from –7 to –10 MPa. Loss of conductivity was between 95–100% in P. lentiscus and between 50–90% in Q. coccifera. Finally, during Phase 4, all seedlings lost their resprouting capacity and died when xil was close to –8 MPa or lower in P. lentiscus and –10 MPa or lower in Q. coccifera.
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In order to analyse the effect of leaf dieback on the capacity of the xylem to supply water to leaves, the LSC was corrected for the reduction in leaf area (LSCcorr) that plants suffered with the decrease in
xil (Fig. 6). P. lentiscus did not lose leaves until xil reached –5 MPa; as a consequence, LSC and LSCcorr decreased in a similar way. When xil fell to –5 MPa, leaf abscission took place and LSCcorr showed slightly higher values than LSC. The moderately high values of LSCcorr were the consequence of the loss in the LSC that had previously been very high (55–95%) and, therefore, leaf abscission had little effect on LSC recovery. On the other hand, the gradual leaf abscission in Q. coccifera permitted the maintenance of LSCcorr values similar to the maximum LSC values registered at the beginning of the drought period without loss of conductivity. As a result, the capacity of this species to supply water to leaves remained nearly constant throughout the whole drought period.
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Drought strategies, stomatal conductance and vulnerability to cavitation
Several studies have reported that plants must regulate transpiration through stomatal conductance in order to avoid xylem cavitation and runaway embolism (Sperry and Pockman, 1993; Cochard et al., 1996; Salleo et al., 2000). Jones and Sutherland (1991) proposed that plants could be classified in two different categories according to their stomatal behaviour: (1) plants that regulate stomatal closure to avoid any loss of hydraulic conductivity; and (2) plants that maximize stomatal conductance even if their stomatal behaviour involves some loss of hydraulic conductance. Cavitation avoidance has been interpreted as the consequence of an efficient stomatal control over transpiration (Cochard et al., 1996), but it has also been considered an ideal condition for actively transpiring plants growing in natural conditions (Nardini and Salleo, 2000; Salleo et al., 2000). However, this topic is still being subjected to extensive study (e.g. Hubbard et al., 2001; Cochard et al., 2002; Sperry et al., 2002). The results of this work show that both species maintained an efficient stomatal control with steep decreases in stomatal conductance, well before reaching
crit that would cause the onset of cavitation events. This behaviour could be considered as cavitation avoidance since stomatal closure prevents xylem cavitation (Sperry et al., 1993). The stomatal response observed in both species would be linked to a conservative use of water resources, mainly in Q. coccifera. In fact, both species displayed drought-avoidance strategies, by water-saving in Q. coccifera and by water-spending in P. lentiscus (Levitt, 1980; Vilagrosa et al., 1997; Vilagrosa, 2002). These strategies are frequently reported in species from habitats with strong water limitations (Salleo and Lo Gullo, 1993). This conservative use of resources is further supported by the results of the P–V curves, which showed low cell wall elasticity with high gradients of water potential associated with small losses of cell volume. These results would be in accordance with other authors (Tenhunen et al., 1987; Pereira and Chaves, 1993) who suggested that a prompt response of plants to drought is crucial in order to prevent severe tissue dehydration and plant damage under Mediterranean severe drought conditions.
In addition to the role of stomatal conductance, it has been reported that plants operate near the point at which water potential causes catastrophic xylem dysfunction (Pockman and Sperry, 2000; Sperry et al., 2002). Moreover, Hacke et al. (2000) proposed that plants from arid climates would maintain wider safety margins than plants from moist habitats, and that this will improve the survival during drought periods. Although these observations coincide with the behaviour observed in Q. coccifera, the same does not apply for P. lentiscus, which maintained narrower intervals between md and crit. P. lentiscus takes advantage of episodes with high water availability, and would maintain narrower limits than Q. coccifera with its conservative strategy based on water saving. Furthermore, several studies (Vilagrosa et al., 1997; Fonseca, 1999; Vilagrosa, 2002) have shown that seedlings of Q. coccifera showed higher mortality rates than those of P. lentiscus during the first summer on experimental plots established in semi-arid climate. Therefore, wider safety margins to xylem dysfunction as observed in this study do not always imply higher survival under field conditions. Moreover, the results of this study suggest that it is possible to maintain wide or narrow margins independently of the habitat occupied, since both species are characteristic of the same Mediterranean dry and semi-arid environments. Martínez-Vilalta et al. (2002) obtained similar results with several Mediterranean shrub and tree species that are closely related to the species studied in this work. However, these authors linked wide or narrow margins to water-conducting efficiency and phylogenetic characteristics. The results here do not fully agree with these observations since P. lentiscus, with higher water-conducting efficiency, was the species showing narrow safety margins and high survival under field conditions. The observations of the present study reinforce the idea that the different drought strategies exhibited by the species would establish the safety margins that each species can maintain, since stomatal closure entails a high cost for species to pay for maintaining xylem integrity (Jones, 1998).
LSC maintenance, leaf dieback and survival capacity.
According to Tyree and Ewers (1991) vulnerability to cavitation can be considered the most important physiological parameter explaining drought tolerance in plants. However, this hypothesis has never been tested (Tyree and Zimmermann, 2002). Several studies have related hydraulic failure to leaf shedding (Tyree et al., 1993) or branch dieback (Davis et al., 2002), and Williams et al. (1997) related embolism with seedling mortality in Adenostoma fasciculatum. Moreover, Sperry and Pockman (1993) have reported the existence of a critical value of leaf specific conductance in Betula occidentalis at which a leaf would be in danger of dieback. As far as is known, the limits for leaf dieback, whole plant mortality, and survival capacity have not yet been related to the loss of hydraulic conductivity. The present study shows that leaf dieback started after the plants reached the turgor loss point and the stomata remained closed, when xil decreased below –5 MPa. This fact would represent a mechanism to avoid runaway embolism through the reduction in overall passive water losses (i.e. cuticular transpiration). On the other hand, whereas leaf dieback began at different rates of loss of conductivity (55% and 20% for P. lentiscus and Q. coccifera, respectively), the coincidence in LSC values around 1.1x10–4 kg m–1 s–1 MPa–1 might support the existence of an LSC threshold at which plants cannot properly supply their leaves with water and thus must regulate the leaf biomass. In addition to these results, both species showed similar values of residual transpiration when stomata remained closed (Vilagrosa et al., 2003).
In this study, four phases were identified in relation to loss of conductivity, leaf dieback, resprouting capacity, and seedling mortality (Table 3). During the first two phases, loss of conductivity and leaf dieback did not represent a problem for the species studied, and they continued living after rewatering, even though the loss of conductivity was as high as 95% in P. lentiscus. During Phase 3, both species were able to resprout after rewatering, possibly indicating that the loss of leaf biomass had been excessive and that they needed to recover leaf photosynthetic biomass to be able to survive. However, loss of conductivity in P. lentiscus ranged between 95 and almost 100%, whilst Q. coccifera only lost between 50–90%. Finally, during Phase 4, loss of conductivity was very close to 100% in both species, and they were unable to resprout and died. Therefore, these results show that cavitation can be considered a good predictor of the limits to drought tolerance of both species since they died when loss of conductivity was almost complete. However, several authors (Hacke et al., 2000; Martínez-Vilalta et al., 2002; Tyree and Zimmermann, 2002) have indicated that loss of conductivity could be considered a good predictor for species survival. Contrary to expected results, the higher resistance to xylem cavitation in Q. coccifera was not accompanied by higher survival under field conditions. These results might indicate that the different behaviour evident between both species could be related to differences in drought tolerance beyond xylem resistance to cavitation. Moreover, P. lentiscus with a water-spender strategy maintained its entire leaf biomass until the almost 100% loss of conductivity while Q. coccifera with a water-saver strategy adjusted its leaf biomass to maximize its capacity to supply water to leaves during the whole drought period (Fig. 6). Therefore, P. lentiscus would have to recover hydraulic conductivity to be able to supply water properly to its leaves when conditions of water availability returned again, whereas Q. coccifera would be able to maintain maximum rates of gas exchange with the remaining leaf biomass. But the latter species with lower loss of conductivity (c. 50–90%) would have to produce new leaves to maintain a positive carbon balance after rewatering, e.g. autumn rainfalls (Table 3).
The results of this study cannot explain the underlying mechanisms of such observations. However, both strategies may be related to different morpho-functional traits in both species. P. lentiscus develops a semi-ring-porous softwood whilst Q. coccifera develops a diffuse-porous hardwood (Villar-Salvador, 2000). According to Fahn (1982), it is cheaper to build a xylem structure based on ring-porous softwood than on diffuse-porous hardwood, and the formation of new vessels can be decoupled from phloem formation quicker in ring-porous (several days) than in diffuse-pore species (several weeks). Consequently, the construction of new vessels in P. lentiscus would suppose lower energy expenditures than in Q. coccifera. In this sense, a good correlation has been observed between starch metabolism and cambium activity in Q. coccifera, indicating a high construction cost for new vessels (Arianoutsou-Faraggitaki et al., 1984). These observations agree with Hacke et al. (2001) who found that higher resistance to cavitation would be related to higher wood density for resisting the mechanical strength generated at low water potentials and, consequently, to a higher construction cost of the xylem. In addition, it has been observed that P. lentiscus is more plastic than Q. coccifera in response to drought conditions. This species was able to modify above and below-ground biomass, and increase leaf water storage and photochemical efficiency under conditions of drought (Vilagrosa et al., 1997, 2003; Rubio et al., 2001). On the other hand, the type of root system developed by both species could also contribute to the observed results. P. lentiscus developed a dense root system along the soil profile while Q. coccifera developed a deep but sparse root system (Vilagrosa et al., 1997; Vilagrosa, 2002). In semi-arid environments, a dense root system can take advantage of small rainfall episodes improving water adsorption and permitting a better rehydration after summer drought (Canadell and Zedler, 1995). In this sense, Fonseca (1999) observed under field conditions that P. lentiscus was able to show higher water potentials than Q. coccifera after autumn rainfalls. In addition to these observations, recent studies have shown that xylem refilling associated with high water potentials could be one of the mechanisms for restoring hydraulic conductivity after xylem cavitation (Salleo et al., 1996; Tyree et al., 1999; Cochard et al., 2001; Vogt, 2001). Therefore, the higher water potentials, as observed in P. lentiscus could facilitate the mechanisms of xylem refilling or the construction of new xylem in this species. This fact would allow the species to maintain its entire leaf biomass until the almost 100% loss of conductivity.
In conclusion, the results of this study indicated that, before the onset of cavitation events, both species maintained an efficient stomatal control linked to a conservative use of water resources. However, wide safety margins do not always imply higher survival rates under field conditions. The results obtained in this study introduce the idea that, independent of the habitat occupied, the drought strategies exhibited by the different species could establish the safety margins that each species can maintain.
According to previous studies, loss of conductivity could be considered a good predictor of survival limits in both species since they both died when the loss of conductivity was very close to 100%. But higher resistance to xylem cavitation was not accompanied by higher survival under field conditions, and it is postulated that this fact could be related to the mopho-functional traits developed for the species. This study also reports the existence of a leaf specific conductivity threshold below which plants cannot supply water to their leaves properly and must regulate leaf biomass to avoid runaway embolism. It would be desirable in order to determine the exact role of xylem cavitation in the resistance of plants to drought by combining field observations on survival, xylem-refilling processes and root system features, with those on vulnerability to cavitation.
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We thank Dr Stephen D Davis of Natural Science Division (Pepperdine University, California) for his helpful suggestions, and two anonymous referees who read the manuscript and provided useful comments. We also thank SIA-DGA technical support and Jacqueline Scheiding for the language corrections of the manuscript. This work was supported by the European Commission REDMED project (ENV4-CT97-0682), and the Conselleria de Medi Ambient (Generalitat Valenciana) R&D project on Vegetation Restoration in the Valencian Region. CEAM is funded by the Generalitat Valenciana and Bancaja.
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