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Constraints on transpiration from an evergreen oak tree in southern Portugal
Agricultural and Forest Meteorology 122 (2004) 193–205
Constraints on transpiration from an evergreen oak tree in southern Portugal T.S. David a,∗ , M.I. Ferreira b , S. Cohen c , J.S. Pereira b , J.S. David b a
Estação Florestal Nacional, INIAP, Av. da República, Quinta do Marquˆes, 2780-159 Oeiras, Portugal b Instituto Superior de Agronomia, Tapada da Ajuda, 1394-017 Lisboa, Portugal c Institute of Soil, Water and Environmental Sciences, P.O. Box 6, Bet Dagan 50250, Israel Received 6 January 2003; accepted 23 September 2003
Abstract The experiment took place at a sparse evergreen oak woodland in southern Portugal. Seasonal courses of sap flow, measured in eight points of the stem of a Quercus rotundifolia tree, were monitored during a 2-year period. Plant water relations (predawn and midday leaf water potential, canopy conductance and whole-plant hydraulic conductance) as well as meteorological variables were also measured during the experimental period (May 1996–August 1998). All evidence showed that the plants remained well watered throughout the observation period. The highest transpiration rates occurred during the summer, when only vestigial amounts of rain fell on the shallow soil with a low water storage capacity. This could only be explained by the direct access of the root system to a 13 m deep water table. Although there was no increase in water stress during the summer drought, the transpiration rates showed an upper limit well below the atmospheric evaporative demand. This was consistent with the occurrence of a maximum limit for the root water uptake capacity determined by the summer value of whole-plant hydraulic conductance and by stomatal control, which prevented leaf water potential from falling below a cavitation threshold. © 2003 Elsevier B.V. All rights reserved. Keywords: Quercus rotundifolia; Transpiration; Sap flow; Canopy conductance; Hydraulic conductance; Groundwater table
1. Introduction The evergreen oak woodlands (montado in Portugal and dehesa in Spain) cover an area of about 2–2.5 million ha in the Iberian Peninsula (Castro et al., 1998). They are mainly located in the southern regions of Portugal and Spain, occupying critical areas in terms of soil and water resources, with low rainfall and high evaporative demand during the summer. These man-made savannah-type ecosystems, charac∗ Corresponding author. Tel.: +351-21-4463737; fax: +351-21-4463702. E-mail address: [email protected] (T.S. David).
terised by a widely separated tree stratum associated with understory of herbs and shrubs, are frequently exploited for agroforestry. The dominant tree species are Quercus suber L. and Quercus rotundifolia Lam. (syn. Quercus ilex spp. rotundifolia). In South Portugal, Q. suber dominates the western and moister areas whereas Q. rotundifolia occupies the drier eastern inland areas. This geographical distribution seems to reflect different tolerances to drought between species. In recent years, both degraded soils and recurrent droughts have been considered as the main causes for enhanced tree mortality, although some pathogens are thought to amplify climatic pressures (David et al., 1992; Santos and Sousa, 1997; Pereira et al., 1999).
0168-1923/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.agrformet.2003.09.014
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Long-term sustainability of these agroforestry systems may be further threatened in the future by regional climatic changes due to global warming. Within the next 80 years rainfall is predicted to decline 13, 31 and 19% during spring, summer and winter, respectively, and air temperature is expected to increase 1.7–5.5 ◦ C (Hulme et al., 1999). In view of these concerns, it is of crucial importance to improve the understanding of the water relations of the tree component of montados, namely its tolerance to drought. Some research on this subject has been reported by Infante et al. (1997) in Q. ilex stands in South Spain and by Oliveira et al. (1992) in Q. suber stands in South Portugal. However, much has yet to be learnt on the function of these ecosystems in order to support the implementation of a suitable management program, aiming at long lasting sustainability. Two main working objectives/hypotheses were initially put forward to frame the purposes of this research: (a) Characterise the seasonal patterns of tree transpiration and infer different possible sources of water supply to the root system. We hypothesised the use of deep sources of water in addition to soil water. (b) Characterise the processes involved in the control of water use by trees, particularly during the summer drought. We hypothesised that possible restrictions in summer transpiration could be explained by hydraulic constraints in the flow path from roots to leaves. The study was conducted in southern Portugal (Alentejo), where tree transpiration and related parameters and variables were monitored during a 2-year period. Given the structure of the vegetation, with very sparse tree cover, e.g. 85% of the holm oak montados have 10–30% tree cover (DGF, 2001) with 30–60 trees per ha (Castro et al., 1998), the functioning of the tree component can be approximated as the sum of individuals. The study concentrated on a single Q. rotundifolia tree considering that when tree crowns are widely separated forest cover may be best represented by isolated trees (Green, 1993). However, the representativeness of the studied tree was checked by comparing its water status with those of two neighbouring trees.
2. The study area The study took place, between May 1996 and August 1998, at the “Herdade da Mitra” experimental area (38◦ 32 N, 8◦ 01 W, 243 m a.s.l.) located near Évora, some 150 km southeast of Lisbon, Portugal. Site topography is slightly undulating. Forest vegetation consists of a sparse and scattered Q. rotundifolia stand, with 35–45 trees ha−1 and a canopy cover of about 39%. The wide and shallow shape of the crowns reflects the traditional pruning performed to increase acorn production and shade for cattle. The understory consists of a mixture of shrubs and grasses, dominated by Cistus spp., grazed by goats and sheep. The climate is Mediterranean with hot and dry summers. Long-term (1951–1980) mean rainfall is 665 mm per year (90% from late autumn to early spring), open water evaporation is 1760 mm per year (INMG, 1991), and mean annual air temperature is 15 ◦ C, ranging from 8.6 ◦ C in January to 23.1 ◦ C in August. During the experiment rainfall was 31% higher than average. The soil is a very shallow (30 cm deep) sandy Cambisol (FAO, 1988) overlying a fractured gneiss rock. Soil water retention capacity is rather low. Maximum available water storage in the soil profile is 24 mm.
3. Methods 3.1. Theoretical framework It is important to recognise that these oak woodlands have a low decoupling coefficient (McNaughton and Jarvis, 1983) due to the small size of the leaves and to the well-ventilated characteristics of the tree crowns. In a similar Q. ilex stand near Seville (Spain), Infante et al. (1997) found average values for the leaf and tree decoupling coefficient (Ω) of 0.2 and 0.035, respectively. For this rough vegetation (low Ω), transpiration (E, kg m−2 s−1 ) is approximated by: ρ cp E = gc D , (1) λγ where gc is the canopy conductance (m s−1 ) which mainly depends on the average leaf stomatal conductance (gs ) and on the leaf area index (L), D is the
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vapour pressure deficit (Pa), ρ is the density of air (kg m−3 ), cp is the specific heat of air (J kg−1 K−1 ), γ is the psychrometric constant (Pa K−1 ) and λ is the latent heat of evaporation (J kg−1 ) (McNaughton and Jarvis, 1983; Jarvis and McNaughton, 1986; Granier et al., 1996; Infante et al., 1997). Transpiration and canopy conductance either can be expressed per unit of ground area or per unit of canopy projected area. Change in the reference area basis, can be easily performed by taking into consideration the average stand canopy cover (0.39). Water transport from soil/groundwater to leaves may be described by Darcy’s law (Hubbard et al., 1999; Sperry, 2000):
leaf area (256 m2 ) was obtained from sub-samples where the ratio of fresh mass/leaf area was assessed. A LI-3000 (LI-Cor, Lincoln, NE, USA) area meter was used for leaf area measurements. Tree leaf area index was 2.6 considering the crown-projected area. Sapwood cross-sectional area was estimated as 6.1 × 10−2 m2 (see Section 3.5). The Huber value, i.e. the ratio of sapwood to leaf area, was 2.38 × 10−4 . Tree age was estimated to be 90 years by counting annual growth rings in a trunk section near the base of the trunk. An estimation of the extension of the root system was achieved, at the end of the study, by excavating a trench 2 m deep and 14 m long centred on the tree trunk.
F = kh (Ψs − Ψl ),
3.3. Meteorological data
(2)
where F is the xylem sap flow (kg m−2 s−1 ), kh is the total hydraulic conductance in the flow path from roots to leaves (kg m−2 s−1 MPa−1 ), Ψ s is the water potential at the supply sources to roots (soil water or groundwater) (MPa) and Ψ l is the leaf water potential (MPa). When the soil–plant continuum is in steady-state, the transpiration flux (E) equals the hydraulic flux (F) and Eqs. (1) and (2) can be combined (Bond and Kavanagh, 1999; Ewers et al., 2000; Sperry, 2000): ρ cp E = F = gc D = kh (Ψs − Ψl ). (3) λγ Eq. (3) can be rewritten to give the canopy resistance (rc = 1/gc ) as a function of D: ρ cp ρ cp D= D, (4) rc = λγE λγ kh (Ψs − Ψl )
An automatic weather station was installed at the site on the top of a 12 m high metallic tower (5 m above the canopy). Solar radiation (CM6B, Kipp and Zonen, Delft, The Netherlands), dry and wet bulb temperatures (aspirated psychrometer H301, Vector Instruments, Rhyl, UK), wind velocity (anemometer A100R, Vector Instruments, Rhyl, UK), wind direction (wind vane W200P, Vector Instruments, Rhyl, UK) and gross rainfall (tipping-bucket rain gauge recorder ARG100, Environmental Measurements, Gateshead, UK) were recorded at 10 min intervals in a CR10 data-logger (Campbell Scientific, Shepshed, UK), powered by a solar panel (SOP10, Solarex, Maryland, USA). Air vapour pressure deficit was calculated from dry and wet bulb temperatures. Power supply to the psychrometer was provided by car batteries.
which demonstrates the link between canopy resistance and hydraulic variables (kh , Ψ s and Ψ l ).
3.4. Groundwater table
3.2. Plant material Following a survey of stand mean tree diameter, crown projected area and tree height, a sample Q. rotundifolia Lam. tree was selected with a stem diameter at breast height of 0.48 m, a crown projected area of 98.5 m2 and a tree height of 6.8 m. This tree was 19 m away from the nearest neighbouring tree. After completion of the transpiration measurements, tree leaf area was estimated by destructive sampling. All leaves were stripped and their fresh mass weighed (approximately 118 kg). Total projected
Groundwater depth was determined from a 25 m deep borehole dug down into the ground. Digging took place during September 1998, at the end of the summer period when the water table is usually at its lowest. An unconfined aquifer was found 13 m below the soil surface. Groundwater was located at a highly fractured and permeable rock layer, between 13 and 15 m depth. 3.5. Sap flow Sap flow (F) was monitored continuously with sap flux density measurements using the thermal
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dissipation method (Granier, 1985, 1987a) from September 1996 to August 1998. Eight sensors (UP GmbH, Landshut, Germany) were radially inserted into the xylem measuring in four different azimuthal orientations (a pair of sensors per orientation). Each sap flow sensor consisted of two probes, 2 cm long, inserted in trunk sapwood at breast height, approximately 10 cm apart. The upper probe was heated to constant power using car batteries and regulating power supply units (UP GmbH, Landshut, Germany). The lower reference probe remained at trunk temperature. The copper–constantan thermocouples of both probes were connected together by the constantan wires, in order to give their temperature difference directly. Sap flow density was calculated according to Granier (1985), considering the thermal difference between probes occurring at times of positive (T) and zero flow (Tmax ). Tmax was calculated for each 10–15-day period. All sensors were connected to CR10 data-loggers (Campbell Scientific) scanning T values every 10 s and recording 10 min averages. Power supply to the data-loggers was provided by solar panels (SOP10, Solarex, Maryland, USA). Tree sap flow density was computed as the mean value measured by the eight sensors. A new set of sensors was installed in the middle of the study period, April 1997, as it was assumed that probes would deteriorate with time. No significant differences were observed between the new and the old sets of sensors. In order to calculate sap flow (F), the sap flow density must be multiplied by sapwood conductive area (Granier, 1985, 1987b). The radial profile of sap velocity at six depths, 48 mm into the xylem, was measured by the heat pulse method (Cohen et al., 1985; Cohen, 1994). Eight sets of probes were installed in the xylem with a 45◦ spacing during a week of measurements. Details of the system are given elsewhere (Cohen, 1994). In order to investigate the possible occurrence of flow beyond this length, three of the sensors were inserted 1 cm deeper into the xylem for a few days. Density and specific heat of sapwood were measured on cores taken from neighbouring trees, and thermal diffusivity of wood was determined when no convective heat transport took place, i.e. from midnight to 4 a.m. The sapwood conductive area was estimated to correspond to a 48 mm xylem depth (estimation error lower than 4%). This value was confirmed at the end
of the study by direct measurement of the wet area of sapwood immediately after cutting. Comparisons of sap flow data from the Granier and the heat pulse methods (for a 2-day overlapping period) showed that although the radial distribution of sap flow density was non-uniform over the conductive area the Granier method provided a good estimate for the average sap flow density over the entire conductive area. The mean tree sap flow was thus computed throughout the experimental period as the product of sap flow density (obtained by the Granier method) and the sapwood conductive area. Tree transpiration (E) was considered equal to sap flow (F) for daily totals and for midday values, when steady-state conditions can be assumed to prevail. Both E and F were expressed per unit of crown-projected area (kg m−2 s−1 or mm per day or mm h−1 ). These values can be converted to a ground area reference basis when multiplied by the average stand canopy cover (0.39). 3.6. Leaf and xylem water potential Leaf water potential (Ψ l ) was measured with a Scholander pressure chamber (PMS 1000, PMS Institute, Corvallis, OR, USA) (Scholander et al., 1965) from May 1996 to August 1998. Six to eight sun-exposed and shaded leaves were sampled in the crown, at least on a 15–21-day basis, just prior to dawn (predawn leaf water potential, Ψ l,p ) and at around 1300 h solar time (midday leaf water potential, Ψ l,m ). In order to assess the representativeness of the sampled tree water status, two neighbouring trees were also monitored for predawn leaf water potential during the experimental period. Daily time-courses of leaf water potential were performed on 2 days (6 May and 25 August 1998). Midday xylem water potential (Ψ x,m ) was also measured in two summer days (19 August 1997 and 25 August 1998) on a sample of eight leaves, covered with aluminium foil-coated bags several hours prior to measurement. 3.7. Stomatal and canopy conductance Stomatal conductance (gs ) was measured every 2 h, from sunrise to sunset, on some days when predawn leaf water potential was measured. A steady-state porometer with a cuvette aperture of 0.6 cm2 (LI-1600,
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LI-COR, Lincoln, NE, USA) was used. As Q. rotundifolia leaves are hypostomatous, measurements were made on the abaxial face. Mean tree stomatal conductance was calculated from a sample of 12 sun-exposed and 12 shaded leaves randomly chosen from different parts of the crown. Due to great variability in individual leaf porometer measurements, these data were only used for the qualitative assessment of daytime patterns of gs variation, but not for quantification purposes. Canopy conductance (gc ) at midday was estimated from sap flow and D data (Eq. (1)), for all days of observation. It was expressed relative to the crown-projected area (mm s−1 ). 3.8. Hydraulic conductance Estimates of whole-tree (soil-to-leaves) hydraulic conductance (kh ) during the course of the experiment were made from measurements of midday sap flow (Fm ), midday leaf water potential (Ψ l,m ) and predawn leaf water potential (Ψ l,p ) (considered equal to the water potential at the supply sources to the roots (Ψ s )), following Eq. (2): Fm kh = . (5) Ψs − Ψl,m Whole-tree hydraulic resistance (rh = 1/kh ) was also calculated as the negative slope of the linear regression between leaf water potential and sap flow (Cochard et al., 1996; Tognetti et al., 1996; Cohen et al., 1997; Wullschleger et al., 1998), for 2 days when time-courses of leaf water potential were available (see Eq. (2)). Hydraulic conductance (kh ) was expressed relative to the crown-projected area (kg m−2 s−1 MPa−1 ). The crown-specific values of kh can be, if wanted, easily converted into leaf-specific or sapwood-specific values by simply taking into account the crown, leaf and sapwood areas given in Section 3.2. 4. Results 4.1. Seasonal trends of tree transpiration and sources of water supply Fig. 1 shows the seasonal patterns of daily transpiration (E), solar radiation (Rs ) and gross rainfall (Rg )
Fig. 1. Seasonal trends of (a) daily transpiration, (b) solar radiation, (c) vapour pressure deficit and (d) rainfall, from September 1996 to August 1998. Transpiration is expressed per unit of crown-projected area.
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as well as of daily average vapour pressure deficit (D), from September 1996 to August 1998. Daily transpiration, estimated from sap flow measurements, ranged from 0.1 to 3.0 mm per day, relative to the crown-projected area, or from 0.04 to 1.2 mm per day, if expressed on a ground area basis. Total transpiration for the 2-year experimental period was of 1061 mm per unit of crown-projected area, or 414 mm per unit of ground area. The corresponding cumulative rainfall was 1735 mm. Daily transpiration reached a peak in summer and declined in winter following closely the seasonal time-course of solar radiation and vapour pressure deficit (Fig. 1). Transpiration trends mainly correlate with meteorological conditions (R = 0.93 with Rs and R = 0.81 with D) and water availability did not seem to become an increasingly limiting factor as summer drought progressed (Fig. 1). This is also supported by the poor relationship observed between daily transpiration (E), expressed as a fraction of solar radiation (Rs ), and predawn leaf water potential (Ψ l,p ) (Fig. 2). Predawn leaf water potential remained relatively high throughout summer, above −0.75 MPa. Data of Fig. 2 show that standardised transpiration (E/Rs ) was almost constant throughout the experimental period, independently of Ψ l,p . These results suggest that Ψ l,p was never low enough to induce major reductions in transpiration during summer. This must also be the case for the surrounding trees, since there was a close relationship, with slope close to 1, between predawn leaf water potentials of the study tree and of its two neighbours (Fig. 3). The root system was well developed both laterally and in depth. The lateral spread of tree roots in the
Fig. 2. Relationship between the daily ratio of transpiration to solar radiation (E/Rs ) and predawn leaf water potential (Ψ l,p ). Transpiration was calculated on a crown coverage basis.
Fig. 3. Relationships between predawn leaf water potentials (Ψ l,p ) of the studied tree and those of two neighbouring trees, denoted by open and closed circles.
shallow soil extended far beyond the crown projection limits. Thick taproots were observed penetrating down through the bedrock cracks either at the trunk base or deriving from lateral shallow roots. At a 2 m depth, a significant number of large roots penetrated deeper into the gneiss rock. 4.2. Hydraulic limits to transpiration rates Although results showed that there was no progressive reduction in daily transpiration due to water stress during the summer periods, there was strong evidence of an upper boundary for sap flow rates (≈0.2 mm h−1 ), which remained constant throughout the experimental period (Fig. 4). Fig. 4 shows 10 min average sap flow rates (for all days of observation) plotted against solar radiation and vapour pressure deficit values at 10, 12 and 16 h (UT) when stomatal conductance, solar radiation and D usually peaked, respectively. From morning to afternoon, there was a progressive loss in the sensitivity of sap flow to radiation: a linear relation at 10 changed to a saturation type curve at 16. The relationship between sap flow and D was asymptotic at all times and remarkably constant over all the different day periods. At midday, steady-state conditions usually prevail and sap flow can be considered equal to the transpiration rate. Eq. (1) was then used to calculate midday canopy conductance (gc ) from sap flow and D data.
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Fig. 4. Relationships between sap flow rate and solar radiation (Rs ) and between sap flow rate and vapour pressure deficit (D), at 10, 12 and 16 h (UT). Sap flow is expressed per unit of crown-projected area.
The relationship between midday canopy conductance and vapour pressure deficit showed a progressive stomatal closure as D increased (Fig. 5). During hot summer periods, when midday transpiration rates remained approximately constant for vapour pressure deficits higher than ca. 1.5 kPa (Fig. 4), the relationship between midday canopy resistance (rc ) and D was linear (Fig. 6). Data for a hot and dry summer day (Fig. 7) suggest that maximum sap flow rates plateau from midmorning to late in the afternoon and that this plateau corresponds to a stable minimum Ψ l of ca. −3 MPa (Fig. 7c). Stomatal closure started when maximum sap flow and minimum leaf water potential values were reached (Fig. 7a).
Fig. 5. Relationship between midday canopy conductance (gc ) and vapour pressure deficit (D), for all the period of observations.
The seasonal patterns of soil water potential near the roots (Ψ s ), taken as the predawn leaf water potential, and of midday leaf water potential (Ψ l,m ) are shown in Fig. 8. Data show that Ψ s varied little compared to Ψ l,m and the seasonal variations in the sap flow driving force ((Ψs − Ψl,m ); see Eq. (2)) were mainly determined by variations in Ψ l,m (Fig. 8). Midday leaf water potential decreased from winter to summer, reaching an absolute minimum of around −3 MPa (Fig. 8). This minimum value was the same during the three consecutive summer periods (Fig. 8). When Ψ l,m was at its minimum (−3 MPa) the xylem water potential (Ψ x,m ) was of about −2 MPa, as measured in
Fig. 6. Linear relationship between midday canopy resistance (rc ) and vapour pressure deficit (D) for selected summer days with D > 1.5 kPa.
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Fig. 9. Seasonal variation of total plant hydraulic conductance (kh , on a crown coverage basis, estimated from Eq. (5)).
19 August 1997 and 25 August 1998. In the summer, the sap flow driving force (Ψs − Ψl,m ) remained fairly constant, around an average of 2.5 MPa (see Fig. 8). The seasonal variation of total hydraulic conductance of the studied Q. rotundifolia tree (Fig. 9) showed that kh varied during the wetter periods (late autumn to early spring; with the highest values occurring after significant rainfall events), but remained fairly constant during the drier and hotter periods. The approximately constant value of kh during the summer was of ca. 2.34 × 10−5 kg m−2 s−1 MPa−1 (equivalent to 0.90 × 10−5 and 0.038 kg m−2 s−1 MPa−1 per unit of leaf and sapwood area, respectively). The whole-tree hydraulic conductance (kh ) was also Fig. 7. Diurnal variation of (a) stomatal conductance (gs ), (b) sap flow and (c) leaf water potential for a hot and dry summer day (25 August 1998). Vertical bars indicate the standard deviations.
Fig. 8. Seasonal variation of soil/groundwater potential (Ψ s ) (considered equal to predawn leaf water potential) and midday leaf water potential (Ψ l,m ), from May 1996 to August 1998.
Fig. 10. Relationships between leaf water potential and sap flow (expressed on a crown coverage basis) for 6 May and 25 August 1998. Total hydraulic resistance (rh = 1/kh ), in the flow path from soil/groundwater to leaves, is the negative of the slope of regression lines.
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estimated from linear regression for 2 days when daily courses of Ψ l and F were measured, 6 May and 25 August 1998 (a late spring and a summer day, respectively) (Fig. 10), yielding kh values of 2.26 × 10−5 kg m−2 s−1 MPa−1 for 6 May and of 2.36 × 10−5 kg m−2 s−1 MPa−1 for 25 August. 5. Discussion 5.1. Access to water and drought avoidance All evidence shows that plants remained well supplied with water throughout the 2-year observation period, with the highest transpiration rates occurring during the dry summer. Although the bulk of the results were obtained from measurements done on a single tree, data of Fig. 3 show that the studied tree reproduces well the water status of other neighbouring trees. The absence of progressive water stress during the summer drought is not uncommon in Mediterranean forests as reported in a long-term sap flow study conducted in Laurus azorica in Tenerife (Jiménez et al., 1996). However, these results are not compatible with the low summer rainfall and the small water storage capacity of the shallow soils (estimated to be 24 mm), which should be depleted within 1 week at the rates of transpiration occurring during summer (3 mm per day). Tree roots must thus have direct access to the 13 m deep water table in order to sustain the summer transpiration when the upper soil dries out. The groundwater reservoir is located at a highly fractured and permeable rock layer, which may be indicative of small seasonal water table fluctuations. Under such conditions, the occurrence of long lasting anaerobic conditions in the upper layers is unlikely, allowing the development and the maintenance of a deep root system. The small variation in water potential near the roots during the study period (Fig. 8) is consistent with the direct access of roots to the water table, suggesting a continued water supply from the groundwater (Zhang et al., 1999). These results may not be totally surprising as it has been reported that woody plants that grow well into summer drought frequently depend on the ability to tap water from permanent water tables (Canadell et al., 1996). The proportion of biomass allocated
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to below-ground tissues is usually increased as the environment becomes more severe (Canadell et al., 1999). Rooting depth can be as high as 53 m in deserts (Canadell et al., 1996). The mean maximum rooting depth for sclerophyllous Mediterranean trees (including mainly Eucalyptus spp. and Quercus spp.) was estimated as 12.6 m by Canadell et al. (1996). Deep rooting seems particularly important for the survival of evergreen trees that must survive a dry season (Breman and Kessler, 1995). The horizontal colonisation of soil by shallow roots, far beyond the crown width, seems also an important adaptation to severe environmental conditions (Breman and Kessler, 1995). The results of our work suggest that the strong root system development, in depth and laterally, is an important strategy for tree survival in the hot and dry conditions of the South Iberian Peninsula. The direct access of the root systems to permanent water tables will allow, whenever possible, a more efficient use of the scarce local water resources by plants. It is not known how general this situation is at a regional scale. However, the results of a recent study show that water table is usually not very deep (4 m on average) in the region of montados (Chambel, 2000, personal communication), which suggests that direct root access to groundwater is probably not uncommon. Moreover, the apparent better tolerance of Q. rotundifolia to drought, in relation to Q. suber, may be attributed more to differences in depth and spread of root systems than to differences in responses at the leaf level, which were found to be negligible (Faria et al., 1998). Hydraulic lift, i.e. water movement from deep to shallow roots at night when surface soils are dry, has been found to play an important role in the ecology and water relations of other dryland ecosystems (Ishikawa and Bledsoe, 2000; Caldwell et al., 1998). This water transfer process has never been studied in montados or dehesas. However, it should be taken into account in future studies as an additional possible cause for the maintenance of tree transpiration and tree survival during the summer drought. 5.2. Hydraulic limits to transpiration rates Sap flow rates were, in this study, considered equal to transpiration rates when steady-state conditions could be assumed to occur: for daily values and at midday. The good linear relationships between Ψ l and
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F (Fig. 10) (Cohen et al., 1983; Wullschleger et al., 1998) and the small height of the trees (≈7 m) suggest that the root and trunk capacitances were small. Furthermore, data of Fig. 7 show that steady-state conditions clearly occur at midday, particularly in summer, since both Ψ l and F were then maintained almost constant from midmorning to midafternoon. Similar to the findings of this work (Fig. 4), many other studies in forests report response curves of transpiration saturating above a certain level of D (Granier et al., 1996; Hogg and Hurdle, 1997; Hogg et al., 1997; Infante et al., 1997; Alsheimer et al., 1998; Anfodillo et al., 1998; Zhang et al., 1999). These curves may be interpreted as the result of a gradual stomatal closure as D increases (as observed in Figs. 5 and 6), supporting a mechanism to maintain constant E. Mott and Parkhurst (1991), Monteith (1995) and Lhomme et al. (1998) contend that stomata respond to the rate of transpiration rather than to humidity per se. The shape of the gc vs. D relationship and the range of variation of gc values found in this study (Fig. 5) are similar to those reported for other temperate, Mediterranean and tropical forests (Granier et al., 1996; Hogg and Hurdle, 1997; Tognetti et al., 1998a; Sellin, 2001). Another possible interpretation of the asymptotic shape of the E vs. D curves is that closing of stomata maintains water potential above a critical threshold, protecting the xylem from catastrophic cavitation. This will impose an internal hydraulic limit in the flow path from roots to leaves that will ultimately determine the maximum transpiration rate that can be sustained by the plant (Hogg and Hurdle, 1997; Hogg et al., 1997). These two apparently alternative approaches can be unified if, as suggested by some recent works, gc vs. D relationships are mainly determined by hydraulic parameters (Oren et al., 1999; Cohen and Naor, 2002) (see also Eq. (4)). Sap flow transport rate (F) between soil/groundwater and the leaves, described by Eq. (2), depends on kh and (Ψs − Ψl ). Seasonally, the hydraulic conductance (kh ) of the studied tree varied between two distinct levels during the rainy periods (late autumn to early spring); but remained constant, at the lower level, during late spring to early autumn (Fig. 9). The variation of kh during the wetter periods may be ascribed to the successive activation/deactivation of water absorption by the shallow surface roots. This should be a short-lived process considering the intermittent
occurrence of rainfall and the low water retention capacity of the shallow soil (24 mm). When the surface soil dries out, only the deep roots with direct access to the permanent water table will remain active, stabilising kh at the lower level. This is what seems to be happening throughout the dry and hot summers. While Ψ s values remained fairly constant throughout the study period, midday Ψ l (Ψ l,m ) varied strongly from winter to summer reaching a repeatedly consistent absolute minimum, around −3 MPa, in summer (Fig. 8). A similar absolute minimum value of Ψ l in field conditions was reported by Faria et al. (1998) for a different Q. rotundifolia stand. Actual minimum values of Ψ l experienced in field conditions are usually considered a cavitation threshold (Ψ c ) (Cochard et al., 1996; Salleo et al., 2000; Sperry, 2000), corresponding to the need of protection from Ψ l falling below that critical level. Vulnerability curves of evergreen Mediterranean oaks (Q. suber and Q. ilex) confirm that a leaf water potential of −3 MPa (approximately equivalent to a xylem water potential of −2 MPa) corresponds to the onset of xylem embolism in these species (Tyree and Cochard, 1996; Tognetti et al., 1998b), when xylem hydraulic conductivity starts to decline. There is always a safety margin between these Ψ c values and complete xylem embolism (Sperry, 2000). Ψ c is a species-specific value (Tyree and Sperry, 1989) being much higher in well watered than in drought-adapted species (Sperry, 2000; Lemoine et al., 2001). The plateau of maximum sap flow rates (around 0.2 mm h−1 ) (Fig. 4) occurred in summer when D was highest (Fig. 1). During most of the summer periods kh , Ψ s and Ψ l,m remained almost constant (Figs. 8 and 9). The maximum value of F (Fmax ) occurred in summer when Ψ l,m reached its minimum (Ψl,m ≈ Ψc ) (see Eq. (2)). The higher kh values during some wetter/colder periods are not relevant for the definition of Fmax since the evaporation rate is then reduced due to the low values of radiation and vapour pressure deficit (Fig. 1) and to the fact that Ψ c is not reached in such conditions (Fig. 8). Water loss through transpiration (E), regulated by stomata and driven by atmospheric demand, cannot exceed the maximum supply by sap flow (Jackson et al., 2000). Thus, a maximum value of summer F (Fmax ) will impose an equal value for E (Emax ). If Emax exceeds Fmax the decrease in Ψ l below Ψ c becomes
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uncontrolled and catastrophic cavitation may cause a complete loss of hydraulic conductance in the xylem (Tyree and Sperry, 1988). During the summer periods, when transpiration was approximately constant at its maximum (E = Emax ) and D was high, there was a very good linear relationship between midday canopy resistance (rc ) and D with an intercept close to zero (Fig. 6). This agrees with what should be theoretically expected from Eq. (4) for constant E. According to Eq. (4), the slope of the rc vs. D relationship can also be calculated from the approximately constant summer values of kh (≈ 2.34 × 10−5 kg m−2 s−1 MPa−1 ) and (Ψs − Ψl ) (≈2.5 MPa). The slope of the linear relationship obtained from this last approach (slope = ρcp /λγkh (Ψs − Ψl ) = 0.128), is almost identical to the adjusted value of the linear regression of Fig. 6 (slope = 0.125). However, this coincidence may partially be a consequence of the use of the same sap flow dataset in the estimation of both rc and kh . It would be interesting in the future to validate this with totally independent rc and kh data. Nevertheless, these results suggest that the response of summer midday canopy resistance to D can be determined from hydraulic parameters alone, as argued by Cohen and Naor (2002). The observed maximum plateau of summer transpiration may, therefore, be ultimately explained by the hydraulic constraints in the flow path from roots to leaves. The role of stomata during such dry periods seems to be the maintenance of the integrity of the conducting system preventing leaf water potential from falling below the cavitation threshold (Tyree and Sperry, 1989; Jones and Sutherland, 1991; Buckley and Mott, 2002). Whatever the mechanisms, stomata can then be envisaged as the plant pressure regulators (Jackson et al., 2000; Buckley and Mott, 2002; Cochard et al., 2002). Results obtained by Salleo et al. (2000) in Laurus nobilis further suggest that stomata closure may not be related to a negative feedback response to Ψ l but rather triggered when the cavitation threshold is reached. Data in Fig. 7 seem to support this for our study during the summer periods. Stomatal conductance of different species has been successfully modelled by linking hydraulic flux to transpiration flux (see Eq. (3)) and maintaining Ψ l above Ψ c (Bond and Kavanagh, 1999). According to Jackson et al. (2000), there is growing evidence that root transport is most often the limiting
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factor of the hydraulic flux. In our study case, the value of the summer hydraulic conductance was certainly dependent on the number and depth of roots tapping water from the aquifer. The possible occurrence of hydraulic lift may also play a role in the maintenance of summer kh . Thus, the absolute value of observed maximum transpiration rate depended on the local species, soil, and hydrogeological conditions, defining a single set of kh , Ψ s and Ψ c values during the summer drought. This same theoretical framework has been useful in explaining the occurrence of different transpiration rates (i.e. different kh and/or Ψ c values) depending on tree species, moisture conditions and stand age (Cohen et al., 1983; Mencuccini and Grace, 1996; Hubbard et al., 1999; Sperry, 2000; Jackson et al., 2000). Plant survival and differences in drought tolerance between species may also correlate with hydraulic limits (Sperry, 2000; Lemoine et al., 2001). It seems a powerful, simple and versatile tool when root water uptake capacity is a limiting factor. This is clearly the case of our study during summer when maximum actual transpiration rates (around 3 mm per day relative to the crown projected area, or 1.2 mm per day on a ground area basis) are well below the atmospheric demand (frequently more than 10 mm per day as estimated by the Penman–Monteith equation). However, when root water uptake capacity exceeds the evaporative demand, no hydraulic limits are imposed to transpiration and midday stomatal conductance is then determined by other factors (e.g. meteorological variables), as observed during the wetter periods of our experiment.
6. Conclusions Tree survival in climates with a long dry season often relies on the access and use of water in deep soil horizons. In this study, we showed that even though the Q. rotundifolia tree had access to a large water reservoir through an extensive root system, the maximum rates of water loss in summer were well below the atmospheric evaporative demand. The restriction seemed to be the result of the lower summer whole-plant hydraulic conductance. As the minimum leaf water potential approached the threshold of xylem cavitation in summer, stomatal closure imposed an additional barrier to water flux preventing catastrophic loss on the water transport capacity. These findings
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should help to develop a sustainable management of evergreen oak woodlands based on the assumptions that (a) tree survival in those environments depends upon the access to a large soil volume, even to groundwater, through an extensive root system and (b) stand density in the more arid zones should be adjusted according to background water availability, which depends on water storage between years. Our results further suggest that the prediction of summer tree transpiration in montados may be certainly improved in the future by taking into account the hydraulic constraints in the root–leaf flow path.
Acknowledgements Thanks to Professor M. Madeira and Professor A. Fabião for their help in the soil and root work and to J. Mendes and H. Miguel for technical assistance in the field experiments. The authors also thank the University of Évora (particularly Professor L. Gazarini) for permission to do field work. Projects PAMAF 4005 and PRAXIS XXI/AGR/3/3.2/2187/95 of the Portuguese Government supported the research. References Alsheimer, M., Köstner, B., Falge, E., Tenhunen, J.D., 1998. Temporal and spatial variation in transpiration of Norway spruce stands within a forested catchment of the Fichtelgebirge, Germany. Ann. Sci. For. 55, 103–123. Anfodillo, T., Rento, S., Carraro, V., Furlanetto, L., Urbinati, C., Carrer, M., 1998. Tree water relations and climatic variations at the alpine timberline: seasonal changes of sap flux and xylem water potential in Larix decidua Miller, Picea abies (L.) Karst. and Pinus cembra (L.). Ann. Sci. For. 55, 159–172. Bond, B.J., Kavanagh, K.L., 1999. Stomatal behaviour of four woody species in relation to leaf-specific hydraulic conductance and threshold water potential. Tree Physiol. 19, 503–510. Breman, H., Kessler, J.J., 1995. Woody plants in agro-ecosystems of semi-arid regions. In: Advanced Series in Agricultural Sciences 23. Springer-Verlag, Berlin, 340 pp. Buckley, T.N., Mott, K.A., 2002. Stomatal water relations and the control of hydraulic supply and demand. Prog. Bot. (Ecol.) 63, 309–325. Caldwell, M.M., Dawson, T.E., Richards, J.H., 1998. Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113, 151–161. Canadell, J., Jackson, R.B., Ehleringer, J.R., Mooney, H.A., Sala, O.E., Schulze, E.D., 1996. Maximum rooting depth of vegetation types at the global scale. Oecologia 108, 583–595.
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Constraints on transpiration from an evergreen oak tree in southern Portugal T.S. David a,∗ , M.I. Ferreira b , S. Cohen c , J.S. Pereira b , J.S. David b a
Estação Florestal Nacional, INIAP, Av. da República, Quinta do Marquˆes, 2780-159 Oeiras, Portugal b Instituto Superior de Agronomia, Tapada da Ajuda, 1394-017 Lisboa, Portugal c Institute of Soil, Water and Environmental Sciences, P.O. Box 6, Bet Dagan 50250, Israel Received 6 January 2003; accepted 23 September 2003
Abstract The experiment took place at a sparse evergreen oak woodland in southern Portugal. Seasonal courses of sap flow, measured in eight points of the stem of a Quercus rotundifolia tree, were monitored during a 2-year period. Plant water relations (predawn and midday leaf water potential, canopy conductance and whole-plant hydraulic conductance) as well as meteorological variables were also measured during the experimental period (May 1996–August 1998). All evidence showed that the plants remained well watered throughout the observation period. The highest transpiration rates occurred during the summer, when only vestigial amounts of rain fell on the shallow soil with a low water storage capacity. This could only be explained by the direct access of the root system to a 13 m deep water table. Although there was no increase in water stress during the summer drought, the transpiration rates showed an upper limit well below the atmospheric evaporative demand. This was consistent with the occurrence of a maximum limit for the root water uptake capacity determined by the summer value of whole-plant hydraulic conductance and by stomatal control, which prevented leaf water potential from falling below a cavitation threshold. © 2003 Elsevier B.V. All rights reserved. Keywords: Quercus rotundifolia; Transpiration; Sap flow; Canopy conductance; Hydraulic conductance; Groundwater table
1. Introduction The evergreen oak woodlands (montado in Portugal and dehesa in Spain) cover an area of about 2–2.5 million ha in the Iberian Peninsula (Castro et al., 1998). They are mainly located in the southern regions of Portugal and Spain, occupying critical areas in terms of soil and water resources, with low rainfall and high evaporative demand during the summer. These man-made savannah-type ecosystems, charac∗ Corresponding author. Tel.: +351-21-4463737; fax: +351-21-4463702. E-mail address: [email protected] (T.S. David).
terised by a widely separated tree stratum associated with understory of herbs and shrubs, are frequently exploited for agroforestry. The dominant tree species are Quercus suber L. and Quercus rotundifolia Lam. (syn. Quercus ilex spp. rotundifolia). In South Portugal, Q. suber dominates the western and moister areas whereas Q. rotundifolia occupies the drier eastern inland areas. This geographical distribution seems to reflect different tolerances to drought between species. In recent years, both degraded soils and recurrent droughts have been considered as the main causes for enhanced tree mortality, although some pathogens are thought to amplify climatic pressures (David et al., 1992; Santos and Sousa, 1997; Pereira et al., 1999).
0168-1923/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.agrformet.2003.09.014
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Long-term sustainability of these agroforestry systems may be further threatened in the future by regional climatic changes due to global warming. Within the next 80 years rainfall is predicted to decline 13, 31 and 19% during spring, summer and winter, respectively, and air temperature is expected to increase 1.7–5.5 ◦ C (Hulme et al., 1999). In view of these concerns, it is of crucial importance to improve the understanding of the water relations of the tree component of montados, namely its tolerance to drought. Some research on this subject has been reported by Infante et al. (1997) in Q. ilex stands in South Spain and by Oliveira et al. (1992) in Q. suber stands in South Portugal. However, much has yet to be learnt on the function of these ecosystems in order to support the implementation of a suitable management program, aiming at long lasting sustainability. Two main working objectives/hypotheses were initially put forward to frame the purposes of this research: (a) Characterise the seasonal patterns of tree transpiration and infer different possible sources of water supply to the root system. We hypothesised the use of deep sources of water in addition to soil water. (b) Characterise the processes involved in the control of water use by trees, particularly during the summer drought. We hypothesised that possible restrictions in summer transpiration could be explained by hydraulic constraints in the flow path from roots to leaves. The study was conducted in southern Portugal (Alentejo), where tree transpiration and related parameters and variables were monitored during a 2-year period. Given the structure of the vegetation, with very sparse tree cover, e.g. 85% of the holm oak montados have 10–30% tree cover (DGF, 2001) with 30–60 trees per ha (Castro et al., 1998), the functioning of the tree component can be approximated as the sum of individuals. The study concentrated on a single Q. rotundifolia tree considering that when tree crowns are widely separated forest cover may be best represented by isolated trees (Green, 1993). However, the representativeness of the studied tree was checked by comparing its water status with those of two neighbouring trees.
2. The study area The study took place, between May 1996 and August 1998, at the “Herdade da Mitra” experimental area (38◦ 32 N, 8◦ 01 W, 243 m a.s.l.) located near Évora, some 150 km southeast of Lisbon, Portugal. Site topography is slightly undulating. Forest vegetation consists of a sparse and scattered Q. rotundifolia stand, with 35–45 trees ha−1 and a canopy cover of about 39%. The wide and shallow shape of the crowns reflects the traditional pruning performed to increase acorn production and shade for cattle. The understory consists of a mixture of shrubs and grasses, dominated by Cistus spp., grazed by goats and sheep. The climate is Mediterranean with hot and dry summers. Long-term (1951–1980) mean rainfall is 665 mm per year (90% from late autumn to early spring), open water evaporation is 1760 mm per year (INMG, 1991), and mean annual air temperature is 15 ◦ C, ranging from 8.6 ◦ C in January to 23.1 ◦ C in August. During the experiment rainfall was 31% higher than average. The soil is a very shallow (30 cm deep) sandy Cambisol (FAO, 1988) overlying a fractured gneiss rock. Soil water retention capacity is rather low. Maximum available water storage in the soil profile is 24 mm.
3. Methods 3.1. Theoretical framework It is important to recognise that these oak woodlands have a low decoupling coefficient (McNaughton and Jarvis, 1983) due to the small size of the leaves and to the well-ventilated characteristics of the tree crowns. In a similar Q. ilex stand near Seville (Spain), Infante et al. (1997) found average values for the leaf and tree decoupling coefficient (Ω) of 0.2 and 0.035, respectively. For this rough vegetation (low Ω), transpiration (E, kg m−2 s−1 ) is approximated by: ρ cp E = gc D , (1) λγ where gc is the canopy conductance (m s−1 ) which mainly depends on the average leaf stomatal conductance (gs ) and on the leaf area index (L), D is the
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vapour pressure deficit (Pa), ρ is the density of air (kg m−3 ), cp is the specific heat of air (J kg−1 K−1 ), γ is the psychrometric constant (Pa K−1 ) and λ is the latent heat of evaporation (J kg−1 ) (McNaughton and Jarvis, 1983; Jarvis and McNaughton, 1986; Granier et al., 1996; Infante et al., 1997). Transpiration and canopy conductance either can be expressed per unit of ground area or per unit of canopy projected area. Change in the reference area basis, can be easily performed by taking into consideration the average stand canopy cover (0.39). Water transport from soil/groundwater to leaves may be described by Darcy’s law (Hubbard et al., 1999; Sperry, 2000):
leaf area (256 m2 ) was obtained from sub-samples where the ratio of fresh mass/leaf area was assessed. A LI-3000 (LI-Cor, Lincoln, NE, USA) area meter was used for leaf area measurements. Tree leaf area index was 2.6 considering the crown-projected area. Sapwood cross-sectional area was estimated as 6.1 × 10−2 m2 (see Section 3.5). The Huber value, i.e. the ratio of sapwood to leaf area, was 2.38 × 10−4 . Tree age was estimated to be 90 years by counting annual growth rings in a trunk section near the base of the trunk. An estimation of the extension of the root system was achieved, at the end of the study, by excavating a trench 2 m deep and 14 m long centred on the tree trunk.
F = kh (Ψs − Ψl ),
3.3. Meteorological data
(2)
where F is the xylem sap flow (kg m−2 s−1 ), kh is the total hydraulic conductance in the flow path from roots to leaves (kg m−2 s−1 MPa−1 ), Ψ s is the water potential at the supply sources to roots (soil water or groundwater) (MPa) and Ψ l is the leaf water potential (MPa). When the soil–plant continuum is in steady-state, the transpiration flux (E) equals the hydraulic flux (F) and Eqs. (1) and (2) can be combined (Bond and Kavanagh, 1999; Ewers et al., 2000; Sperry, 2000): ρ cp E = F = gc D = kh (Ψs − Ψl ). (3) λγ Eq. (3) can be rewritten to give the canopy resistance (rc = 1/gc ) as a function of D: ρ cp ρ cp D= D, (4) rc = λγE λγ kh (Ψs − Ψl )
An automatic weather station was installed at the site on the top of a 12 m high metallic tower (5 m above the canopy). Solar radiation (CM6B, Kipp and Zonen, Delft, The Netherlands), dry and wet bulb temperatures (aspirated psychrometer H301, Vector Instruments, Rhyl, UK), wind velocity (anemometer A100R, Vector Instruments, Rhyl, UK), wind direction (wind vane W200P, Vector Instruments, Rhyl, UK) and gross rainfall (tipping-bucket rain gauge recorder ARG100, Environmental Measurements, Gateshead, UK) were recorded at 10 min intervals in a CR10 data-logger (Campbell Scientific, Shepshed, UK), powered by a solar panel (SOP10, Solarex, Maryland, USA). Air vapour pressure deficit was calculated from dry and wet bulb temperatures. Power supply to the psychrometer was provided by car batteries.
which demonstrates the link between canopy resistance and hydraulic variables (kh , Ψ s and Ψ l ).
3.4. Groundwater table
3.2. Plant material Following a survey of stand mean tree diameter, crown projected area and tree height, a sample Q. rotundifolia Lam. tree was selected with a stem diameter at breast height of 0.48 m, a crown projected area of 98.5 m2 and a tree height of 6.8 m. This tree was 19 m away from the nearest neighbouring tree. After completion of the transpiration measurements, tree leaf area was estimated by destructive sampling. All leaves were stripped and their fresh mass weighed (approximately 118 kg). Total projected
Groundwater depth was determined from a 25 m deep borehole dug down into the ground. Digging took place during September 1998, at the end of the summer period when the water table is usually at its lowest. An unconfined aquifer was found 13 m below the soil surface. Groundwater was located at a highly fractured and permeable rock layer, between 13 and 15 m depth. 3.5. Sap flow Sap flow (F) was monitored continuously with sap flux density measurements using the thermal
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dissipation method (Granier, 1985, 1987a) from September 1996 to August 1998. Eight sensors (UP GmbH, Landshut, Germany) were radially inserted into the xylem measuring in four different azimuthal orientations (a pair of sensors per orientation). Each sap flow sensor consisted of two probes, 2 cm long, inserted in trunk sapwood at breast height, approximately 10 cm apart. The upper probe was heated to constant power using car batteries and regulating power supply units (UP GmbH, Landshut, Germany). The lower reference probe remained at trunk temperature. The copper–constantan thermocouples of both probes were connected together by the constantan wires, in order to give their temperature difference directly. Sap flow density was calculated according to Granier (1985), considering the thermal difference between probes occurring at times of positive (T) and zero flow (Tmax ). Tmax was calculated for each 10–15-day period. All sensors were connected to CR10 data-loggers (Campbell Scientific) scanning T values every 10 s and recording 10 min averages. Power supply to the data-loggers was provided by solar panels (SOP10, Solarex, Maryland, USA). Tree sap flow density was computed as the mean value measured by the eight sensors. A new set of sensors was installed in the middle of the study period, April 1997, as it was assumed that probes would deteriorate with time. No significant differences were observed between the new and the old sets of sensors. In order to calculate sap flow (F), the sap flow density must be multiplied by sapwood conductive area (Granier, 1985, 1987b). The radial profile of sap velocity at six depths, 48 mm into the xylem, was measured by the heat pulse method (Cohen et al., 1985; Cohen, 1994). Eight sets of probes were installed in the xylem with a 45◦ spacing during a week of measurements. Details of the system are given elsewhere (Cohen, 1994). In order to investigate the possible occurrence of flow beyond this length, three of the sensors were inserted 1 cm deeper into the xylem for a few days. Density and specific heat of sapwood were measured on cores taken from neighbouring trees, and thermal diffusivity of wood was determined when no convective heat transport took place, i.e. from midnight to 4 a.m. The sapwood conductive area was estimated to correspond to a 48 mm xylem depth (estimation error lower than 4%). This value was confirmed at the end
of the study by direct measurement of the wet area of sapwood immediately after cutting. Comparisons of sap flow data from the Granier and the heat pulse methods (for a 2-day overlapping period) showed that although the radial distribution of sap flow density was non-uniform over the conductive area the Granier method provided a good estimate for the average sap flow density over the entire conductive area. The mean tree sap flow was thus computed throughout the experimental period as the product of sap flow density (obtained by the Granier method) and the sapwood conductive area. Tree transpiration (E) was considered equal to sap flow (F) for daily totals and for midday values, when steady-state conditions can be assumed to prevail. Both E and F were expressed per unit of crown-projected area (kg m−2 s−1 or mm per day or mm h−1 ). These values can be converted to a ground area reference basis when multiplied by the average stand canopy cover (0.39). 3.6. Leaf and xylem water potential Leaf water potential (Ψ l ) was measured with a Scholander pressure chamber (PMS 1000, PMS Institute, Corvallis, OR, USA) (Scholander et al., 1965) from May 1996 to August 1998. Six to eight sun-exposed and shaded leaves were sampled in the crown, at least on a 15–21-day basis, just prior to dawn (predawn leaf water potential, Ψ l,p ) and at around 1300 h solar time (midday leaf water potential, Ψ l,m ). In order to assess the representativeness of the sampled tree water status, two neighbouring trees were also monitored for predawn leaf water potential during the experimental period. Daily time-courses of leaf water potential were performed on 2 days (6 May and 25 August 1998). Midday xylem water potential (Ψ x,m ) was also measured in two summer days (19 August 1997 and 25 August 1998) on a sample of eight leaves, covered with aluminium foil-coated bags several hours prior to measurement. 3.7. Stomatal and canopy conductance Stomatal conductance (gs ) was measured every 2 h, from sunrise to sunset, on some days when predawn leaf water potential was measured. A steady-state porometer with a cuvette aperture of 0.6 cm2 (LI-1600,
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LI-COR, Lincoln, NE, USA) was used. As Q. rotundifolia leaves are hypostomatous, measurements were made on the abaxial face. Mean tree stomatal conductance was calculated from a sample of 12 sun-exposed and 12 shaded leaves randomly chosen from different parts of the crown. Due to great variability in individual leaf porometer measurements, these data were only used for the qualitative assessment of daytime patterns of gs variation, but not for quantification purposes. Canopy conductance (gc ) at midday was estimated from sap flow and D data (Eq. (1)), for all days of observation. It was expressed relative to the crown-projected area (mm s−1 ). 3.8. Hydraulic conductance Estimates of whole-tree (soil-to-leaves) hydraulic conductance (kh ) during the course of the experiment were made from measurements of midday sap flow (Fm ), midday leaf water potential (Ψ l,m ) and predawn leaf water potential (Ψ l,p ) (considered equal to the water potential at the supply sources to the roots (Ψ s )), following Eq. (2): Fm kh = . (5) Ψs − Ψl,m Whole-tree hydraulic resistance (rh = 1/kh ) was also calculated as the negative slope of the linear regression between leaf water potential and sap flow (Cochard et al., 1996; Tognetti et al., 1996; Cohen et al., 1997; Wullschleger et al., 1998), for 2 days when time-courses of leaf water potential were available (see Eq. (2)). Hydraulic conductance (kh ) was expressed relative to the crown-projected area (kg m−2 s−1 MPa−1 ). The crown-specific values of kh can be, if wanted, easily converted into leaf-specific or sapwood-specific values by simply taking into account the crown, leaf and sapwood areas given in Section 3.2. 4. Results 4.1. Seasonal trends of tree transpiration and sources of water supply Fig. 1 shows the seasonal patterns of daily transpiration (E), solar radiation (Rs ) and gross rainfall (Rg )
Fig. 1. Seasonal trends of (a) daily transpiration, (b) solar radiation, (c) vapour pressure deficit and (d) rainfall, from September 1996 to August 1998. Transpiration is expressed per unit of crown-projected area.
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as well as of daily average vapour pressure deficit (D), from September 1996 to August 1998. Daily transpiration, estimated from sap flow measurements, ranged from 0.1 to 3.0 mm per day, relative to the crown-projected area, or from 0.04 to 1.2 mm per day, if expressed on a ground area basis. Total transpiration for the 2-year experimental period was of 1061 mm per unit of crown-projected area, or 414 mm per unit of ground area. The corresponding cumulative rainfall was 1735 mm. Daily transpiration reached a peak in summer and declined in winter following closely the seasonal time-course of solar radiation and vapour pressure deficit (Fig. 1). Transpiration trends mainly correlate with meteorological conditions (R = 0.93 with Rs and R = 0.81 with D) and water availability did not seem to become an increasingly limiting factor as summer drought progressed (Fig. 1). This is also supported by the poor relationship observed between daily transpiration (E), expressed as a fraction of solar radiation (Rs ), and predawn leaf water potential (Ψ l,p ) (Fig. 2). Predawn leaf water potential remained relatively high throughout summer, above −0.75 MPa. Data of Fig. 2 show that standardised transpiration (E/Rs ) was almost constant throughout the experimental period, independently of Ψ l,p . These results suggest that Ψ l,p was never low enough to induce major reductions in transpiration during summer. This must also be the case for the surrounding trees, since there was a close relationship, with slope close to 1, between predawn leaf water potentials of the study tree and of its two neighbours (Fig. 3). The root system was well developed both laterally and in depth. The lateral spread of tree roots in the
Fig. 2. Relationship between the daily ratio of transpiration to solar radiation (E/Rs ) and predawn leaf water potential (Ψ l,p ). Transpiration was calculated on a crown coverage basis.
Fig. 3. Relationships between predawn leaf water potentials (Ψ l,p ) of the studied tree and those of two neighbouring trees, denoted by open and closed circles.
shallow soil extended far beyond the crown projection limits. Thick taproots were observed penetrating down through the bedrock cracks either at the trunk base or deriving from lateral shallow roots. At a 2 m depth, a significant number of large roots penetrated deeper into the gneiss rock. 4.2. Hydraulic limits to transpiration rates Although results showed that there was no progressive reduction in daily transpiration due to water stress during the summer periods, there was strong evidence of an upper boundary for sap flow rates (≈0.2 mm h−1 ), which remained constant throughout the experimental period (Fig. 4). Fig. 4 shows 10 min average sap flow rates (for all days of observation) plotted against solar radiation and vapour pressure deficit values at 10, 12 and 16 h (UT) when stomatal conductance, solar radiation and D usually peaked, respectively. From morning to afternoon, there was a progressive loss in the sensitivity of sap flow to radiation: a linear relation at 10 changed to a saturation type curve at 16. The relationship between sap flow and D was asymptotic at all times and remarkably constant over all the different day periods. At midday, steady-state conditions usually prevail and sap flow can be considered equal to the transpiration rate. Eq. (1) was then used to calculate midday canopy conductance (gc ) from sap flow and D data.
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Fig. 4. Relationships between sap flow rate and solar radiation (Rs ) and between sap flow rate and vapour pressure deficit (D), at 10, 12 and 16 h (UT). Sap flow is expressed per unit of crown-projected area.
The relationship between midday canopy conductance and vapour pressure deficit showed a progressive stomatal closure as D increased (Fig. 5). During hot summer periods, when midday transpiration rates remained approximately constant for vapour pressure deficits higher than ca. 1.5 kPa (Fig. 4), the relationship between midday canopy resistance (rc ) and D was linear (Fig. 6). Data for a hot and dry summer day (Fig. 7) suggest that maximum sap flow rates plateau from midmorning to late in the afternoon and that this plateau corresponds to a stable minimum Ψ l of ca. −3 MPa (Fig. 7c). Stomatal closure started when maximum sap flow and minimum leaf water potential values were reached (Fig. 7a).
Fig. 5. Relationship between midday canopy conductance (gc ) and vapour pressure deficit (D), for all the period of observations.
The seasonal patterns of soil water potential near the roots (Ψ s ), taken as the predawn leaf water potential, and of midday leaf water potential (Ψ l,m ) are shown in Fig. 8. Data show that Ψ s varied little compared to Ψ l,m and the seasonal variations in the sap flow driving force ((Ψs − Ψl,m ); see Eq. (2)) were mainly determined by variations in Ψ l,m (Fig. 8). Midday leaf water potential decreased from winter to summer, reaching an absolute minimum of around −3 MPa (Fig. 8). This minimum value was the same during the three consecutive summer periods (Fig. 8). When Ψ l,m was at its minimum (−3 MPa) the xylem water potential (Ψ x,m ) was of about −2 MPa, as measured in
Fig. 6. Linear relationship between midday canopy resistance (rc ) and vapour pressure deficit (D) for selected summer days with D > 1.5 kPa.
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Fig. 9. Seasonal variation of total plant hydraulic conductance (kh , on a crown coverage basis, estimated from Eq. (5)).
19 August 1997 and 25 August 1998. In the summer, the sap flow driving force (Ψs − Ψl,m ) remained fairly constant, around an average of 2.5 MPa (see Fig. 8). The seasonal variation of total hydraulic conductance of the studied Q. rotundifolia tree (Fig. 9) showed that kh varied during the wetter periods (late autumn to early spring; with the highest values occurring after significant rainfall events), but remained fairly constant during the drier and hotter periods. The approximately constant value of kh during the summer was of ca. 2.34 × 10−5 kg m−2 s−1 MPa−1 (equivalent to 0.90 × 10−5 and 0.038 kg m−2 s−1 MPa−1 per unit of leaf and sapwood area, respectively). The whole-tree hydraulic conductance (kh ) was also Fig. 7. Diurnal variation of (a) stomatal conductance (gs ), (b) sap flow and (c) leaf water potential for a hot and dry summer day (25 August 1998). Vertical bars indicate the standard deviations.
Fig. 8. Seasonal variation of soil/groundwater potential (Ψ s ) (considered equal to predawn leaf water potential) and midday leaf water potential (Ψ l,m ), from May 1996 to August 1998.
Fig. 10. Relationships between leaf water potential and sap flow (expressed on a crown coverage basis) for 6 May and 25 August 1998. Total hydraulic resistance (rh = 1/kh ), in the flow path from soil/groundwater to leaves, is the negative of the slope of regression lines.
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estimated from linear regression for 2 days when daily courses of Ψ l and F were measured, 6 May and 25 August 1998 (a late spring and a summer day, respectively) (Fig. 10), yielding kh values of 2.26 × 10−5 kg m−2 s−1 MPa−1 for 6 May and of 2.36 × 10−5 kg m−2 s−1 MPa−1 for 25 August. 5. Discussion 5.1. Access to water and drought avoidance All evidence shows that plants remained well supplied with water throughout the 2-year observation period, with the highest transpiration rates occurring during the dry summer. Although the bulk of the results were obtained from measurements done on a single tree, data of Fig. 3 show that the studied tree reproduces well the water status of other neighbouring trees. The absence of progressive water stress during the summer drought is not uncommon in Mediterranean forests as reported in a long-term sap flow study conducted in Laurus azorica in Tenerife (Jiménez et al., 1996). However, these results are not compatible with the low summer rainfall and the small water storage capacity of the shallow soils (estimated to be 24 mm), which should be depleted within 1 week at the rates of transpiration occurring during summer (3 mm per day). Tree roots must thus have direct access to the 13 m deep water table in order to sustain the summer transpiration when the upper soil dries out. The groundwater reservoir is located at a highly fractured and permeable rock layer, which may be indicative of small seasonal water table fluctuations. Under such conditions, the occurrence of long lasting anaerobic conditions in the upper layers is unlikely, allowing the development and the maintenance of a deep root system. The small variation in water potential near the roots during the study period (Fig. 8) is consistent with the direct access of roots to the water table, suggesting a continued water supply from the groundwater (Zhang et al., 1999). These results may not be totally surprising as it has been reported that woody plants that grow well into summer drought frequently depend on the ability to tap water from permanent water tables (Canadell et al., 1996). The proportion of biomass allocated
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to below-ground tissues is usually increased as the environment becomes more severe (Canadell et al., 1999). Rooting depth can be as high as 53 m in deserts (Canadell et al., 1996). The mean maximum rooting depth for sclerophyllous Mediterranean trees (including mainly Eucalyptus spp. and Quercus spp.) was estimated as 12.6 m by Canadell et al. (1996). Deep rooting seems particularly important for the survival of evergreen trees that must survive a dry season (Breman and Kessler, 1995). The horizontal colonisation of soil by shallow roots, far beyond the crown width, seems also an important adaptation to severe environmental conditions (Breman and Kessler, 1995). The results of our work suggest that the strong root system development, in depth and laterally, is an important strategy for tree survival in the hot and dry conditions of the South Iberian Peninsula. The direct access of the root systems to permanent water tables will allow, whenever possible, a more efficient use of the scarce local water resources by plants. It is not known how general this situation is at a regional scale. However, the results of a recent study show that water table is usually not very deep (4 m on average) in the region of montados (Chambel, 2000, personal communication), which suggests that direct root access to groundwater is probably not uncommon. Moreover, the apparent better tolerance of Q. rotundifolia to drought, in relation to Q. suber, may be attributed more to differences in depth and spread of root systems than to differences in responses at the leaf level, which were found to be negligible (Faria et al., 1998). Hydraulic lift, i.e. water movement from deep to shallow roots at night when surface soils are dry, has been found to play an important role in the ecology and water relations of other dryland ecosystems (Ishikawa and Bledsoe, 2000; Caldwell et al., 1998). This water transfer process has never been studied in montados or dehesas. However, it should be taken into account in future studies as an additional possible cause for the maintenance of tree transpiration and tree survival during the summer drought. 5.2. Hydraulic limits to transpiration rates Sap flow rates were, in this study, considered equal to transpiration rates when steady-state conditions could be assumed to occur: for daily values and at midday. The good linear relationships between Ψ l and
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F (Fig. 10) (Cohen et al., 1983; Wullschleger et al., 1998) and the small height of the trees (≈7 m) suggest that the root and trunk capacitances were small. Furthermore, data of Fig. 7 show that steady-state conditions clearly occur at midday, particularly in summer, since both Ψ l and F were then maintained almost constant from midmorning to midafternoon. Similar to the findings of this work (Fig. 4), many other studies in forests report response curves of transpiration saturating above a certain level of D (Granier et al., 1996; Hogg and Hurdle, 1997; Hogg et al., 1997; Infante et al., 1997; Alsheimer et al., 1998; Anfodillo et al., 1998; Zhang et al., 1999). These curves may be interpreted as the result of a gradual stomatal closure as D increases (as observed in Figs. 5 and 6), supporting a mechanism to maintain constant E. Mott and Parkhurst (1991), Monteith (1995) and Lhomme et al. (1998) contend that stomata respond to the rate of transpiration rather than to humidity per se. The shape of the gc vs. D relationship and the range of variation of gc values found in this study (Fig. 5) are similar to those reported for other temperate, Mediterranean and tropical forests (Granier et al., 1996; Hogg and Hurdle, 1997; Tognetti et al., 1998a; Sellin, 2001). Another possible interpretation of the asymptotic shape of the E vs. D curves is that closing of stomata maintains water potential above a critical threshold, protecting the xylem from catastrophic cavitation. This will impose an internal hydraulic limit in the flow path from roots to leaves that will ultimately determine the maximum transpiration rate that can be sustained by the plant (Hogg and Hurdle, 1997; Hogg et al., 1997). These two apparently alternative approaches can be unified if, as suggested by some recent works, gc vs. D relationships are mainly determined by hydraulic parameters (Oren et al., 1999; Cohen and Naor, 2002) (see also Eq. (4)). Sap flow transport rate (F) between soil/groundwater and the leaves, described by Eq. (2), depends on kh and (Ψs − Ψl ). Seasonally, the hydraulic conductance (kh ) of the studied tree varied between two distinct levels during the rainy periods (late autumn to early spring); but remained constant, at the lower level, during late spring to early autumn (Fig. 9). The variation of kh during the wetter periods may be ascribed to the successive activation/deactivation of water absorption by the shallow surface roots. This should be a short-lived process considering the intermittent
occurrence of rainfall and the low water retention capacity of the shallow soil (24 mm). When the surface soil dries out, only the deep roots with direct access to the permanent water table will remain active, stabilising kh at the lower level. This is what seems to be happening throughout the dry and hot summers. While Ψ s values remained fairly constant throughout the study period, midday Ψ l (Ψ l,m ) varied strongly from winter to summer reaching a repeatedly consistent absolute minimum, around −3 MPa, in summer (Fig. 8). A similar absolute minimum value of Ψ l in field conditions was reported by Faria et al. (1998) for a different Q. rotundifolia stand. Actual minimum values of Ψ l experienced in field conditions are usually considered a cavitation threshold (Ψ c ) (Cochard et al., 1996; Salleo et al., 2000; Sperry, 2000), corresponding to the need of protection from Ψ l falling below that critical level. Vulnerability curves of evergreen Mediterranean oaks (Q. suber and Q. ilex) confirm that a leaf water potential of −3 MPa (approximately equivalent to a xylem water potential of −2 MPa) corresponds to the onset of xylem embolism in these species (Tyree and Cochard, 1996; Tognetti et al., 1998b), when xylem hydraulic conductivity starts to decline. There is always a safety margin between these Ψ c values and complete xylem embolism (Sperry, 2000). Ψ c is a species-specific value (Tyree and Sperry, 1989) being much higher in well watered than in drought-adapted species (Sperry, 2000; Lemoine et al., 2001). The plateau of maximum sap flow rates (around 0.2 mm h−1 ) (Fig. 4) occurred in summer when D was highest (Fig. 1). During most of the summer periods kh , Ψ s and Ψ l,m remained almost constant (Figs. 8 and 9). The maximum value of F (Fmax ) occurred in summer when Ψ l,m reached its minimum (Ψl,m ≈ Ψc ) (see Eq. (2)). The higher kh values during some wetter/colder periods are not relevant for the definition of Fmax since the evaporation rate is then reduced due to the low values of radiation and vapour pressure deficit (Fig. 1) and to the fact that Ψ c is not reached in such conditions (Fig. 8). Water loss through transpiration (E), regulated by stomata and driven by atmospheric demand, cannot exceed the maximum supply by sap flow (Jackson et al., 2000). Thus, a maximum value of summer F (Fmax ) will impose an equal value for E (Emax ). If Emax exceeds Fmax the decrease in Ψ l below Ψ c becomes
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uncontrolled and catastrophic cavitation may cause a complete loss of hydraulic conductance in the xylem (Tyree and Sperry, 1988). During the summer periods, when transpiration was approximately constant at its maximum (E = Emax ) and D was high, there was a very good linear relationship between midday canopy resistance (rc ) and D with an intercept close to zero (Fig. 6). This agrees with what should be theoretically expected from Eq. (4) for constant E. According to Eq. (4), the slope of the rc vs. D relationship can also be calculated from the approximately constant summer values of kh (≈ 2.34 × 10−5 kg m−2 s−1 MPa−1 ) and (Ψs − Ψl ) (≈2.5 MPa). The slope of the linear relationship obtained from this last approach (slope = ρcp /λγkh (Ψs − Ψl ) = 0.128), is almost identical to the adjusted value of the linear regression of Fig. 6 (slope = 0.125). However, this coincidence may partially be a consequence of the use of the same sap flow dataset in the estimation of both rc and kh . It would be interesting in the future to validate this with totally independent rc and kh data. Nevertheless, these results suggest that the response of summer midday canopy resistance to D can be determined from hydraulic parameters alone, as argued by Cohen and Naor (2002). The observed maximum plateau of summer transpiration may, therefore, be ultimately explained by the hydraulic constraints in the flow path from roots to leaves. The role of stomata during such dry periods seems to be the maintenance of the integrity of the conducting system preventing leaf water potential from falling below the cavitation threshold (Tyree and Sperry, 1989; Jones and Sutherland, 1991; Buckley and Mott, 2002). Whatever the mechanisms, stomata can then be envisaged as the plant pressure regulators (Jackson et al., 2000; Buckley and Mott, 2002; Cochard et al., 2002). Results obtained by Salleo et al. (2000) in Laurus nobilis further suggest that stomata closure may not be related to a negative feedback response to Ψ l but rather triggered when the cavitation threshold is reached. Data in Fig. 7 seem to support this for our study during the summer periods. Stomatal conductance of different species has been successfully modelled by linking hydraulic flux to transpiration flux (see Eq. (3)) and maintaining Ψ l above Ψ c (Bond and Kavanagh, 1999). According to Jackson et al. (2000), there is growing evidence that root transport is most often the limiting
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factor of the hydraulic flux. In our study case, the value of the summer hydraulic conductance was certainly dependent on the number and depth of roots tapping water from the aquifer. The possible occurrence of hydraulic lift may also play a role in the maintenance of summer kh . Thus, the absolute value of observed maximum transpiration rate depended on the local species, soil, and hydrogeological conditions, defining a single set of kh , Ψ s and Ψ c values during the summer drought. This same theoretical framework has been useful in explaining the occurrence of different transpiration rates (i.e. different kh and/or Ψ c values) depending on tree species, moisture conditions and stand age (Cohen et al., 1983; Mencuccini and Grace, 1996; Hubbard et al., 1999; Sperry, 2000; Jackson et al., 2000). Plant survival and differences in drought tolerance between species may also correlate with hydraulic limits (Sperry, 2000; Lemoine et al., 2001). It seems a powerful, simple and versatile tool when root water uptake capacity is a limiting factor. This is clearly the case of our study during summer when maximum actual transpiration rates (around 3 mm per day relative to the crown projected area, or 1.2 mm per day on a ground area basis) are well below the atmospheric demand (frequently more than 10 mm per day as estimated by the Penman–Monteith equation). However, when root water uptake capacity exceeds the evaporative demand, no hydraulic limits are imposed to transpiration and midday stomatal conductance is then determined by other factors (e.g. meteorological variables), as observed during the wetter periods of our experiment.
6. Conclusions Tree survival in climates with a long dry season often relies on the access and use of water in deep soil horizons. In this study, we showed that even though the Q. rotundifolia tree had access to a large water reservoir through an extensive root system, the maximum rates of water loss in summer were well below the atmospheric evaporative demand. The restriction seemed to be the result of the lower summer whole-plant hydraulic conductance. As the minimum leaf water potential approached the threshold of xylem cavitation in summer, stomatal closure imposed an additional barrier to water flux preventing catastrophic loss on the water transport capacity. These findings
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should help to develop a sustainable management of evergreen oak woodlands based on the assumptions that (a) tree survival in those environments depends upon the access to a large soil volume, even to groundwater, through an extensive root system and (b) stand density in the more arid zones should be adjusted according to background water availability, which depends on water storage between years. Our results further suggest that the prediction of summer tree transpiration in montados may be certainly improved in the future by taking into account the hydraulic constraints in the root–leaf flow path.
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