Combining sap flow and trunk diameter measurements to assess water needs in mature olive orchards

Environmental and Experimental Botany 72 (2011) 330–338

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Combining sap flow and trunk diameter measurements to assess water needs in mature olive orchards José Enrique Fernández a,∗ , Félix Moreno a , María José Martín-Palomo b , María Victoria Cuevas a , José Manuel Torres-Ruiz a , Alfonso Moriana b a b

Instituto de Recursos Naturales y Agrobiología (IRNAS-CSIC), Avenida de Reina Mercedes n.◦ 10, 41012 Seville, Spain Escuela Técnica Superior de Ingeniería Agronómica, Departamento de Ciencias Agroforestales, Carretera de Utrera km. 1, 41013 Seville, Spain

a r t i c l e

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Article history: Received 28 July 2010 Received in revised form 11 April 2011 Accepted 17 April 2011 Keywords: Deficit irrigation Maximum trunk diameter Sap flux Signal intensity Tree water consumption

a b s t r a c t Sap flux (Q) and trunk diameter variation (TDV) are among the most useful plant-based measurements to detect water stress and to evaluate plant water consumption. The usefulness of both methods decreases, however, when applied to species that, like olive, have an outstanding tolerance to drought and a remarkable capacity to take up water from drying soils. Evidence shows that this problem is greater in old, big trees with heavy fruit load. Our hypothesis is that the analysis of simultaneous measurements of Q and TDV made in the same trees is more useful for assessing irrigation needs in old olive orchards than the use of any of these two methods alone. To test our hypothesis, we analysed relations between Q, TDV, midday stem water potential ( stem ), relative extractable water and atmospheric demand in an olive orchard of 38-year-old ‘Manzanilla’ trees with heavy fruit load. Measurements were made during one irrigation season (May–October), in fully irrigated trees (FI, 107% of the crop evapotranspiration, ETc , supplied by irrigation), and in trees under two levels of deficit irrigation (DI60, 61% ETc ; DI30, 29% ETc ). Time courses of Q and TDV measured on days of contrasting weather and soil water conditions were analysed to evaluate the usefulness of both methods to assess the crop water status. We calculated the daily tree water consumption (Ep ) from Q measurements. For both DI treatments we calculated a signal intensity by dividing daily Ep values of each DI tree by those of the FI tree (SI−Ep ). We did the same with the maximum daily shrinkage (MDS) values (SI−MDS ). Neither SI−Ep nor SI−MDS rendered useful information for assessing the crop water needs. On the contrary, the daily difference for maximum trunk diameter (MXTD) between each of the DI trees and the FI tree (DMXTD ) clearly indicated the onset and severity of water stress. A similar analysis with the Ep values, from which DEp values were derived, showed the effect of water stress on the water consumption of the trees. We concluded that the simultaneous use of DMXTD and DEp values provides more detailed information to assess water needs in mature olive orchards than the use of Q or TDV records alone. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Vineyards and fruit tree orchards are common in arid and semiarid areas where the lack of water makes compulsory accurate scheduling and precise irrigation management (Fereres and Evans, 2006). This explains the substantial amount of research invested in the last decades into new irrigation technologies and more efficient scheduling approaches, summarized by Jones (2004) and Naor (2006), among others. The assessment of the onset and severity of water stress has been, and still is, an area of interest. For grapevines and fruit trees, sensitive water stress indicators have been derived from measurements of sap flow rate (SF) and diameter changes in conductive organs, normally the trunk.

∗ Corresponding author. Tel.: +34 954 62 47 11x175; fax: +34 954 62 40 02. E-mail address: [email protected] (J.E. Fernández). 0098-8472/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2011.04.004

A variety of methods based on SF measurements has been described both for detecting water stress and assessing crop water needs in grapevines (Ginestar et al., 1998; Fernández et al., 2008a), ˇ citrus (Nadezhdina and Cermák, 1997), and other fruit tree species including olive (Giorio and Giorio, 2003; Nadezhdina et al., 2007; Fernández et al., 2008a,b). Measurements of trunk diameter variations (TDV) have also been used with the same purposes in a variety ˜ et al., 2010). For of species (Fernández and Cuevas, 2010; Ortuno olive, the work by Moriana et al. (2003) in ‘Picual’, Moriana and Fereres (2004) in ‘Picual’ and ‘Arbequina’, Pérez-López et al. (2008a) in ‘Cornicabra’ and Cuevas et al. (2010) in ‘Manzanilla’ showed that the age and size of the tree, and the presence, and load, of fruits, reduce the usefulness of the TDV records both for detecting water stress and assessing water needs. Several authors have explored the relations between SF, TDV and several other indicators of plant water status such as the plant water potential and gas exchange. For fruit tree species we can men-

2. Materials and methods 2.1. Experimental orchard and irrigation treatments

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tion works with peach (Goldhamer et al., 1999; Cohen et al., 2001; ˜ Remorini and Massai, 2003; Conejero et al., 2007), lemon (Ortuno et al., 2006a,b), and plum (Intrigliolo and Castel, 2006). No work of this kind has been made for olive. The physiological processes in which SF and TDV rely, as well as main reasons for agreements and disagreements between simultaneous records of these two plantbased indicators made in the same plant have been pointed out by different authors, as summarized by Drew and Downes (2009) and Fernández and Cuevas (2010), among others. The work by Steppe ˇ et al. (2006, 2008a,b), Cermák et al. (2007) and Sevanto et al. (2008) shows that the water-flow dynamics within a plant can be better understood by combining information from SF and TDV records. Our hypothesis is that the analysis of simultaneous measurements of SF and TDV made in big, old olive trees with heavy fruit load yields more useful information for assessing crop water needs than the use of any of these two methods alone. The aim of this research was to evaluate the usefulness of simultaneous sap flux (Q) and TDV measurements for detecting (a) the onset and severity of water stress in mature ‘Manzanilla’ olive trees with heavy fruit load, and (b) the effect of the tree water stress on its water consumption. We analysed the relations between Q, TDV, midday stem water potential, soil water content and atmospheric demand in an orchard planted with 38-year-old ‘Manzanilla’ olive trees with heavy fruit load.

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The experiments were carried out in a 0.5 ha olive orchard at La Hampa experimental farm, southwest Spain (37◦ 17 N, 6◦ 3 W, 30 m a.s.l.), planted with 38-year-old ‘Manzanilla de Sevilla’ (from now on ‘Manzanilla’) olive trees at 7 m × 5 m spacing. The trees, trained to an open centre canopy of about 4.5 m diameter, have a single trunk and two main branches from 0.7 to 1.5 m above ground. Trees were pruned every January, and the leaf area index reached maximum values of ca. 1.7 in September. The soil is a sandy loam of homogeneous texture, both vertically and horizontally, with mean values of 14.8% clay, 7.0% silt, 4.7% fine sand and 73.5% coarse sand. The upper drained soil water content limit is 0.22 m3 m−3 and the lower soil water content limit is 0.09 m3 m−3 . The soil depth is ca. 2 m. The area has a Mediterranean climate, with a wet, mild season from October to April and a dry, hot season from May to September. Average potential evapotranspiration (ETo ) and precipitation (P) values in the area are 1162.8 mm and 502.1 mm, respectively (period 1971–2006). Experiments were carried out during the irrigation season of 2006 (May 3–October 13), a year with heavy fruit load (‘on’ year). The orchard was divided into three plots, each receiving a different irrigation treatment: (1) FI, full irrigation in which enough water was supplied to replace the crop evapotranspiration (ETc ). The ETc values were calculated by applying the crop coefficient approach. Details are given in Fernández et al. (2006a). The resulting ETc values were used to calculate the daily irrigation dose, ID, as ID = ETc − Pe , being Pe the effective precipitation, estimated as 75% of the P value recorded by the weather station of the farm (see below); (2) DI60, a deficit irrigation treatment consisting in supplying decreasing IDs until severe water stress in the trees, detected by an automatic irrigation controller based on SF measurements (Fernández et al., 2008b). Then the controller applied increasing IDs for a few days, enough to replenish the rootzone, followed by a new period of decreasing IDs. This cycle was repeated before the end of the irrigation season. The total amount of water supplied by irrigation was aimed at 60% of ETc ; and (3) DI30, a more severe deficit irrigation treatment in which decreasing IDs were supplied

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DOY 2006 (120 = May 1) Fig. 1. Daily values of the FAO56 Penman–Monteith potential evapotranspiration (ETo ) calculated from records collected by the weather station at the experimental farm (A); irrigation dose (ID) applied in each treatment and rainfall amounts (R) recorded by the mentioned weather station (B). Also shown are the midday stem water potential values ( stem , n = 6) measured in trees of each treatment (C) and the relative extractable water values (REW, n = 7) derived from soil water measurements around trees of each treatment (D). Vertical bars represent ± the standard error. DOY = day of year.

for most of the pit hardening period, when olive is considered to be less sensitive to water stress (Goldhamer, 1999). Recovery irrigation was applied at the end of August to increase fruit size. Total water supplies in this treatment was aimed at 30% of ETc . For all treatments, irrigation supplies were applied daily by using a lateral per tree row with five 3 L h−1 drippers per tree, 1 m apart. The seasonal courses of the supplied IDs are shown in Fig. 1. 2.2. Sap flow measurements One representative tree per treatment was instrumented with heat-pulse velocity (HPV) probes (Tranzflo NZ Ltd., Palmerston North, New Zealand) for SF measurements by the Tz heat-pulse method (Green et al., 2003). The method was validated for olive by Fernández et al. (2006b). Three sets of probes were installed into the single trunk of each tree. Each set had two temperature probes, located at 5 mm upstream and 10 mm downstream of a linear heater probe. Each temperature probe had four thermocouples, at 5, 12, 22 and 35 mm below the cambium. Heat pulses (60 W over 1 s) were applied once every 30 min. Both the firing of the heat pulses and the recording of the outputs from the probes was made by a CR10X Campbell datalogger (Campbell Scientific Inc, North Logan, USA). The probes were installed on the night of March 27, in places free of scars and other irregularities, all around the trunks. The system was working con-

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tinuously from that day to the end of the irrigation season, on October 13. Outputs were processed as described by Fernández et al. (2006b), and the resulting values of each set of probes were averaged to derive the sap flux in the trunk (Q, L h−1 ), as well as the daily plant water consumption (Ep , L tree−1 day−1 ). For both DI treatments we calculated the signal intensity values for Ep (SI−Ep ) by dividing the Ep values of each DI tree by the Ep values in the FI tree (Goldhamer and Fereres, 2001). We also calculated the daily difference for Ep between the each DI and the FI tree (DEp ). All calculations were made after considering the values recorded at the beginning of the irrigation season as zero. At that time trees of all treatments had a similar water status (Fig. 1C). 2.3. Trunk diameter measurements TDV records were taken in the three trees instrumented with HPV probes. A set of linear variable displacement transducers (LVDT) (Solarton Metrology model DF ± 2.5 mm, accuracy ±10 ␮m, Bognor Regis, UK) was attached to the trunk of each tree with a bracket made of aluminium and Invar, and alloy with a thermal expansion close to zero (Katerji et al., 1994). The LVDTs were installed on the north side of the trunks, at about the same height as the HPV probes. Readings were taken every 10 s with a CR10X Campbell datalogger and an AM416 Campbell multiplexer, and 30 min means were saved. The LVDTs were installed and removed on the same days than the HPV probes. From the TDV records we calculated the maximum daily shrinkage (MDS) as the difference between the maximum (MXTD) and the minimum (MNTD) trunk diameter values recorded on the day. Then we calculated both the daily values of signal intensity for MDS (SI−MDS ) and the daily difference between the DI trees and the FI tree for the MXTD (DMXTD ). Similarly to what we did with the Q data, all calculations were made after considering the values recorded at the beginning of the irrigation season as zero. 2.4. Other measurements Soil water profiles were recorded every 10–20 days throughout the irrigation season in the rootzone of three representative trees of each treatment, including that instrumented with the HPV probes and LVDT sensor. Access tubes for a neutron probe (Troxler 3300, Research Triangle Park, NC, USA) were installed along the tree row, at distances of 0.5, 1.5, and 2.5 m from the trunk in one tree per treatment, and at 1.5 and 2.5 m from the trunk in another two trees per treatment. We used the neutron probe to measure the volumetric soil water content ( v ) in the 0.2–2.0 m soil layer, at 0.1 m depth intervals; values of  v in the top 0.0–0.2 m were determined by gravimetry. With the measured  v values and after Granier (1987) we calculated a depth equivalent of water expressed as the level of relative extractable water (REW). Midday stem water potential ( stem ) was recorded every 5–7 days throughout the irrigation season, using a pressure chamber (Soilmoisture Equipment Corp., Santa Barbara, CA, USA). Two leaves per tree, from the three trees per treatment instrumented with access tubes for the neutron probe (n = 6), were sampled from the base of shoots in the trunk or main branches. Sampled leaves were wrapped in aluminium foil some 2 h before midday. Maximum, minimum, and average values of wind speed and direction, P, global solar radiation (Rs ), PAR radiation, temperature of the air (Ta ) and relative humidity were recorded every 30 min by an automatic Campbell station (Campbell Scientific Ltd., Shepshed, UK), located next to the orchard. Vapour pressure deficit of the air (Da ) was calculated and provided by the software of the station.

2.5. Statistical analysis Differences between treatments for both  stem and REW values were evaluated by applying an analysis of variance (ANOVA; separation of means with the Tukey’s test; statistically significant differences at P < 0.05). 3. Results 3.1. Influence of the irrigation treatment on the plant and soil water status The seasonal courses of ETo and water supplies in the three experimental treatments are shown in Fig. 1A and B, respectively. The resulting  stem and REW values for each treatment are shown in Fig. 1C and D, respectively. In the FI treatment the total amount of water supplied by irrigation amounted to 4427.1 m3 ha−1 (107% ETc ), enough for keeping REW values close to 1 for the whole season, indicating non-limiting soil water conditions all throughout the experimental period. In the DI60 treatment, ID values decreased from May 11, day of year (DOY) 131 to June 25 (DOY 176), and then remained more or less constant until July 17 (DOY 198). The first significant differences (P < 0.05) in REW between the DI60 and the FI treatment appeared on DOY 179. About half of the available soil water in the DI60 treatment was depleted by DOY 200 (REW = 0.47 ± 0.09). Significant differences (P < 0.05) in  stem between the FI and the DI60 trees were detected from DOY 180 to DOY 200 (Fig. 1C). The increased IDs supplied to the DI60 trees from July 18 (DOY 199) to mid September (Fig. 1B), led to REW values greater than 0.8 (Fig. 1D). In agreement with this increase in REW,  stem values of the DI60 trees decreased to values close to those of the FI trees from July 24 (DOY 205) (Fig. 1C). In fact, differences in  stem between the FI and the DI60 trees were not significant from that day to the end of the irrigation season, except on DOYs 209 and 212. The ID60 treatment received a total of 2692.3 m3 ha−1 (61% ETc ). In the DI30 treatment, decreasing IDs were supplied from May 16 (DOY 136) to August 6 (DOY 218). Differences in  stem between the FI and the DI30 trees (Fig. 1C) were significant (P < 0.05) from DOY 191 to a few days after the beginning of the recovery irrigation applied from August 7 to August 20 (Fig. 1B). That irrigation led to non significant differences in  stem between the FI and the DI30 trees from DOY 233 to DOY 240 (Fig. 1C). Decreasing IDs were supplied to the DI30 trees again after the recovery irrigation, from August 21 to the end of the irrigation season on October 13. This caused a new decrease in the  stem values, until the rainfall events in mid September (51.0 mm were recorded from DOY 255 to 266), replenished soil water in the rootzone (Fig. 1D). A total of 1274.2 m3 ha−1 (29% ETc ) was applied in the DI30 treatment. 3.2. Response of Q and TDV to soil and weather conditions Daily courses of Q and TDV values recorded on days of contrasting soil water status and weather conditions are shown in Fig. 2. Fig. 2A shows records from the FI tree on a 6-day-period at the beginning of the irrigation season (DOY 147 = May 27). On those days REW values in the FI treatment were fairly constant (0.88–0.90, Fig. 1D) but both Da and Rs , two main driving variables for Ep , changed dramatically (Fig. 2D). The Q records reflected those changes in the atmospheric demand. From DOY 147 to 149, two days of relatively high values of Da and Rs , we recorded a maximum MDS value of 480 ␮m on DOY 148, and a trunk growth rate (TGR) value of 34 ␮m in the FI tree. From DOY 150 to 152, however, TDV records rendered little information, likely because of the stormy weather on those days (Fig. 1A and B), as discussed in Section 4.1. Fig. 2B shows records from the DI30 tree later in the season,

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DOY 2006 Fig. 2. Time courses of sap flux (Q) and trunk diameter variations (TDV) measured in the experimental trees on days of contrasting weather and soil water conditions. Numbers in A–C represent the daily water consumption (L tree−1 day−1 ) estimated from sap flow measurements. The dashed line in (C) indicates a recovery irrigation made in treatment DI60 on day of year (DOY) 199. D–F show the time courses of the hourly mean values of vapour pressure deficit of the air (Da ) and global solar radiation (Rs ) recorded by the weather station at the experimental farm. Numbers in D–F represent the daily ETo values (mm).

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when REW ≈0.50 and  stem values as low as −1.74 ± 0.09 MPa were recorded on DOY 191 (Fig. 1C and D). Under these conditions of low available water, Q values also echoed the atmospheric demand, similarly to what was observed in the FI trees under non-limiting soil water conditions. We recorded a TGR valued of −197 ␮m in the DI30 from DOY 189 to 192, a period of increasing atmospheric demand and decreasing soil water content (Fig. 1D). The decrease in trunk diameter agreed with the increasing plant water stress (Fig. 1C). However, the trunk radius increased 48 ␮m from DOY 193 to DOY 194, despite of no appreciable change in the soil water status. This was likely due to the decrease in the atmospheric demand on DOY 193. Fig. 2C shows the daily courses of Q and TDV values in the DI60 tree on the days before and after the beginning of the first recovery irrigation on DOY 199. Lower MDS values and greater TGR values were derived from the TDV records after DOY 199 than on the previous days, in agreement with the increasing available water content (Fig. 1D) and the decreasing atmospheric demand (Fig. 2F). The Q values, however, echoed once again the time course of ETo , but were little, if any, affected by the dramatic changes in soil water content from DOY 199. The relation between diurnal courses of Q and TDV recorded in trees of the three treatments is illustrated in Fig. 3. The days shown in the figure had different soil water and weather conditions, summarized in Table S1 and Fig. S1. After dawn Q responded more markedly than TDV, for all conditions. On DOYs 148, 197 and 202, remarkable increases in Q were recorded from early in the morning in all instrumented trees, in agreement with the quick and marked increases both of Da and Rs recorded in those days soon after dawn (Fig. S1). On DOY 150, however, no measurable Q values were detected at 8.00 GMT in the FI trees (Fig. 3B), despite of the high available water in the soil (Fig. 1D, Table S1). This was a cloudy day with very low Rs values (Fig. S1B), so stomata likely remained closed until late on the day. In addition, the low Da values achieved on that day surely contributed to the low recorded Q values. On DOY 236 the maximum Q values were recorded from, and not before, 8.00 GMT. This was likely due to the increase in Da occurring later on that day, as compared to DOYs 148, 197 and 202 (Fig. S1). During the night transpiration in olive is negligible, and sap flow accounts mainly for the refilling of the tree’s capacitance. This explains the low Q values shown in Fig. 3, often below the threshold for

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Q (L h-1) Fig. 3. Relation between diurnal courses of the trunk diameter variation (TDV) and sap flux measured in the trunk (Q) of the experimental trees on days of contrasting weather and soil water conditions, shown in Table S1 and Fig. S1. The dashed lines represent the lowest Q value that can be accurately measured with the used sap flow method. Values recorded at 08.00 Greenwich mean time (GMT) and 13.00 GMT are indicated with arrows. DOY = day of year.

accurate measurements with the HPV method. We usually found some degree of hysteresis between Q and TDV during the day, since greater changes in TDV were recorded late in the afternoon than early in the morning, for the same Q values. This happened except on very humid days such as DOY 150 (Fig. 3B), when the TDV records were useless due to the effect of the high relative humidity of the air on the bark related tissues. The greatest degree of hysteresis was achieved on the days with the most demanding atmospheric conditions, such as DOY 197 (Fig. 3C and Fig. S1C). In the DI60 trees, the hysteresis was greater before (Fig. 3C) than after (Fig. 3D) the recovery irrigation applied on DOY 199.

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Fig. 4 shows the courses of both Q and TDV values recorded in some of the experimental trees on the days shown in Fig. 3. Also shown in the figure are the five phases described by Herzog et al. (1995) when comparing idealized diurnal courses of Q and TDV obtained from the same tree. Phase I corresponds to the trunk diameter increase during the night, when transpiration is negligible and the plant rehydrates. Phase II describes the delay between the increase in Q after sunrise and the shrinking of the trunk. Herzog et al. (1995) mentioned that the sequence of Phases I and II may be reversed when the tree is saturated. This often occurred in our case, even in the DI60 and DI30 trees, especially until ca. DOY 180. From the beginning of the irrigation season to that day the available soil water was relatively high, which could account for the full recovery of the trunk diameter during the night. Phase III goes from the beginning of trunk shrinkage early on the day to the maximum Q value, achieved later. Phase IV corresponds to the delay between the maximum Q value and the minimum trunk diameter, normally achieved in the afternoon. Finally, Phase V describes the delay between the minimum trunk diameter recorded on the day and the minimum Q value which, in our case, was usually recorded soon after sunset. On days of high atmospheric demand (DOYs 148, 197 and 202, Fig. S1), a quick rise of Q was recorded from dawn, followed by a plateau at around midday (Fig. 4). Lower slopes of the increase in Q during the morning were recorded on days of lower atmospheric demand, such as DOYs 150 and 236, and the plateau was much shorter, or even did not exist (Fig. 4).

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DOY 2006 (120 = May 1) Fig. 5. Time courses of the signal intensities derived from the daily transpiration estimated from sap flow measurements, SI−Ep (A), and from the maximum daily shrinkage, SI−MDS (B). The shown values were derived from sap flow and trunk diameter variations measured in the trunk of the experimental trees. See text for details on the measurements and SI calculation.

3.3. Usefulness of the Q- and TDV-derived indices The time courses of the SI−Ep values (Fig. 5A) showed similar trends both for the DI60 and DI30 trees. For both treatments SI−Ep values decreased on the first weeks after the beginning of the irrigation season, in agreement with the decreases in REW (Fig. 1D). Later in the season the SI−Ep values became more stable, showing no clear response to the dramatic changes in the available soil water occurred in both treatments. Contrarily to SI−Ep , the time course of SI−MDS (Fig. 5B) showed a different trend for each DI treatment.

From ca. DOY 180 to DOY 220, when the trees of both treatments showed similar increases in water stress (Fig. 1C), SI−MDS values increased for the DI60 tree but decreased for the DI30 tree (Fig. 5B). The peak SI−MDS values observed in both treatments occurred on days of marked decrease in ETo (Fig. 1A), with no relation either with  stem (Fig. 1C) or REW (Fig. 1D). Contrary to SI−Ep and SI−MDS , the time courses of DMXTD between the DI trees and the FI tree clearly indicated the onset of water stress (Fig. 6). For the DI60 trees, DMXTD decreased from ca. DOY

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DOY 2006 (160 = June 9) Fig. 6. Differences between the maximum trunk diameter (MXTD) derived from TDV measurements in the DI60 (A) and DI30 (B) trees and that of the FI tree recorded on the same day. The shown differences were calculated after considering the values recorded at the beginning of the irrigation season as zero. DOY = day of year.

180 to ca. DOY 199 (Fig. 6A), in agreement with the time courses of the plant (Fig. 1C) and soil water status (Fig. 1D). From DOY 200 to DOY 216, a period of recovery from water stress for the DI60 tree, DMXTD increased. For the rest of the period shown in Fig. 6 DMXTD fluctuated without a clear trend, in accordance to the lack of differences in  stem between the DI60 and the FI trees (Fig. 1C). Fig. 6B shows the DMXTD values for the DI30 tree. In this case DMXTD values also echoed the dynamics of the plant and soil water status. Thus, DMXTD values decreased from ca. DOY 184 to ca. DOY 210, in agreement with the decrease both in  stem (Fig. 1C) and REW (Fig. 1D) recorded in the DI30 treatment on that period. From ca. DOY 210 to 220 the DMXTD values remained about constant, as the  stem values recorded in the DI30 trees. Values of DMXTD increased from DOY 220, in agreement to the recoveries of both the plant and soil water status in the DI30 treatment. The time courses of DEp for both DI treatments are shown in Fig. 7. The Ep values of the DI60 trees were similar to those in the FI tree for most of the season (Fig. 7A), despite the reduced water supplies in the DI treatment (Fig. 1B). The DI30 trees, however, showed negative values of DEp from ca. DOY 185 to ca. DOY 238 (Fig. 7B), in agreement with the dynamics of the plant (Fig. 1C) and soil water status (Fig. 1D). For both DI treatments, the DEp records fluctuated more than the soil and plant water status, perhaps because of sudden changes in ETo (Fig. 1A). 4. Discussion 4.1. Response of Q and TDV to soil and weather conditions In the area of the experimental orchard, as in many Mediterranean areas where the olive tree is grown, most days of the irrigation season are clear-sky days in which both Rs and Da increase quickly during the morning time. The weather station of the farm often recorded maximum Rs values close to 1000 W m−2 at about 12 Greenwich mean time (GMT) or soon after, while Da amounted to ca. 4 kPa or more at about 14–16 GMT. Measurements carried out in the experimental orchard by Fernández et al. (1997) and DiazEspejo et al. (2006) showed that, under these weather conditions, maximum gs values are achieved at about 8–9 GMT. Maximum Q values, however, are usually registered around of even after noon,

-8

DI30-FI

160

170

180

190

200

210

220

230

240

DOY 2006 (160 = June 9) Fig. 7. Differences between the daily transpiration estimated from sap flow measurements (Ep ) in the DI60 (A) and DI30 (B) trees and that of the FI tree recorded on the same day. The shown differences were calculated after considering the values recorded at the beginning of the irrigation season as zero. DOY = day of year.

because of the increase of Da until the mentioned hours (Moreno et al., 1996; Fernández et al., 2001). The fast and marked opening of the olive stomata early in the morning explains the quick increase of Q during the morning time (Figs. 2 and 3). The fact that the daily courses of both Rs and Da influenced markedly the daily dynamics of Q is not surprising either, since both are two main driving variables for Ep . A quicker response of Q to the recovery irrigations, however, could have been expected. Fig. 2C shows that this did not occur, at least for the DI60 tree. Once again, the response of olive stomata to environmental conditions may explain this lack of response. It is known that, for olive, after rewatering, stomatal conductance values take longer to recover than the plant water status, the delay being related to the level of water stress previously reached (Fernández and Moreno, 1999). Fereres et al. (1996) studied the recovery of 22-year-old ‘Picual’ trees after a period of severe water stress in which minimum leaf water potential ( l ) values close to −8.0 MPa were achieved. They found that  l recovered in about four days, but it took several weeks for gs to recover. In addition, the recovery irrigations applied in our orchard did not affect the whole rhizosphere, since water was applied through the localized irrigation system and it is known that roots of the trees in the orchard explore greater soil volumes than those wetted by irrigation (Fernández et al., 1991). Roots remaining in drying soil during the irrigation season, including the recovery irrigation period, might have induced stomatal closure. Evidences on the occurrence of this root-to-shoot signalling mechanism in olive have been reported by Fernández et al. (2003), Pérez-López et al. (2008b) and Cuevas et al. (2010). On a daily basis, the TDV records from the DI60 tree responded quicker and more clearly to the recovery irrigation applied on DOY 199 than the Q values recorded in the same tree (Fig. 2C). The fact that TGR increased and MDS decreased on DOYs 199 and 200 agrees with the decrease in atmospheric demand (Fig. 2F) and with the increase in  stem and REW. But from DOY 201, when ETo increased again, a big increase in MDS was recorded, and TGR decreased, despite of the increasing soil water content (Fig. 1D). This shows that TGR and MDS were influenced not only by the increase in soil water content, but also, and likely more markedly, by the

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weather conditions. This is not surprising, since both Q and TDV, although based on different physiological and plant-related mechanisms (Fernández and Cuevas, 2010), depend closely on the plant water status which, in olive, is strongly related to weather conditions (Fernández and Moreno, 1999; Connor and Fereres, 2005). Differences in the dynamics of Q and TDV records shown in Figs. 2–4 could originate, at least in part, from the fact that TDV was not as markedly affected as Q by the olive stomata behaviour. The fact that on days of low atmospheric demand, such as DOYs 150 and 236, Q increased slower in the morning than on days of greater atmospheric demand, and that the plateau in the central hours of the day was much shorter, or even did not exist, is in agreement with the gs and Q behaviour of the olive tree, commented above. No useful information for the detection of water stress was obtained from the analysis of the five phases described by Herzog et al. (1995) (Fig. 4). We analysed both the length of each of the five described phases and the time of the day at which they occurred versus  stem and REW values, and found no robust relationships (data not shown). To our knowledge, this kind of analysis has not been carried out before for mature olive trees with heavy fruit load. Data collected on rainy days, such as DOY 150, shows another difference between Q and TDV records. The first showed a reduced water consumption, according to the low atmospheric demand, while the TDV records became useless because of the hygroscopic nature of ˜ et al., 2010). the bark tissues (Fernández and Cuevas, 2010; Ortuno 4.2. Potential of Q- and TDV-derived indices for monitoring water stress and water consumption Both the REW and  stem values recorded throughout the irrigation season show that the FI trees were reliable reference trees for the tested Q- and TDV-derived indices. Thus, REW values in the FI treatment were always above 0.8 (Fig. 1D), and midday  stem values were greater than −1.4 MPa (Fig. 1C), a threshold value for water stress in olive trees exhibiting heavy fruit load (A. Moriana, unpublished results). For the two tested DI treatments, the dynamics both of SI−Ep and SI−MDS (Fig. 5) were weakly related to those of the soil and plant water status (Fig. 1). Cuevas et al. (2010) worked in the same orchard and found steady values of SI−MDS until September 9 (DOY 252), when REW < 0.2. The first symptoms of fruit shrivelling appeared 16 days later, which led them to conclude that SI−MDS was useful to detect severe, but not mild, water stress levels. This is in agreement with the poor response of SI−MDS to the water status of the trees shown by our results. Both for SI−Ep and SI−MDS , peak values were more related to changes in ETo than to changes in  stem . To our knowledge, this is the first time the signal intensity approach for Ep has been tested in olive. The fact that differences in SI−MDS between the DI60 and the DI30 trees were greater at the end of the experimental period than at the beginning could have been due, at least in part, to the loss of elasticity in the green tissues of the bark, cambium and outer xylem having been greater in the DI30 tree than in the D60 tree. The influence of seasonal changes in the elasticity of the tissues on the seasonal dynamics of SI−MDS was explored by Sevanto et al. (2003) in Scots pine trees and by Intrigliolo and Castel (2004) in plum. It has been reported that the usefulness of TDV-derived indices as indicators of water stress decreases with plant age, size and the presence, and load, of fruits. The effect of tree size in the MDS vs.  stem relationships was investigated by Intrigliolo and Castel (2006) in 6- to 8-year-old plum trees. Their results show that for tree trunk diameters ranging between 8 cm and 13 cm, MDS increased 13% for each centimetre of increase in trunk diameter, as a result of the thicker phloem tissues of the larger trees. For olive, a species with marked alternate bearing, Moriana et al. (2003) reported a big effect of fruit load in the seasonal pattern

of trunk growth in mature ‘Picual’ olive trees under non-limiting soil water conditions: while trees with a light fruit load (‘off’ year) grew steadily throughout the dry season at an increasing rate, trees with heavy fruit load (‘on’ year) grew very slowly after the beginning of the fruits growing period. They found negligible values of trunk diameter increase in trees growing under water deficit conditions. In fully irrigated 5/6-year-old ‘Cornicabra’ olive trees, Pérez-López et al. (2008a) found steady TGR values during midsummer in the non-fruiting year, and decreasing values in the fruiting year. Tognetti et al. (2009) found wide temporal fluctuations of TGR throughout the season in 15/16-year-old ‘Nocellara del Belice’ olive trees. They reported no significant differences in TGR recorded in trees under different water treatments. Differences in MDS among treatments were not clear either. Their experimental orchard, however, was in a relatively humid area with a short dry season, in which severe water stress conditions rarely occurred. The signal intensity approach has been proven useful to monitor the onset of water stress in a variety of fruit trees (Fernández and ˜ et al., 2010). Poor results, however, have been Cuevas, 2010; Ortuno reported for grapevines (Intrigliolo and Castel, 2007b) and olive (Cuevas et al., 2010). Our results also show that the signal intensity approach, when applied to Ep and MDS data, is not useful to detect the onset of water stress in mature ‘Manzanilla’ olive trees with heavy fruit load. On the contrary, DMXTD seems to be a sensitive index for water stress. Thus, the seasonal course of DMXTD (Fig. 6) agreed with that of  stem (Fig. 1C), for both DI treatments. Goldhamer and Fereres (2001) and Moriana and Fereres (2002) reported, for peach and olive trees respectively, that in young, well-watered trees, trunk growth throughout the season was reflected in MXTD as well as in MNTD records, making these variables potentially useful indicators for irrigation scheduling. It has been reported, however, that the usefulness of TDV records for irrigation scheduling decreases when the fruits become a dominant sink (Intrigliolo and Castel, 2007a, in plum; Intrigliolo and Castel, 2007b, in grapevines). Our data show that the DMXTD records, in spite of having been taken in old, big trees with heavy fruit load, were useful to detect the onset, and severity, of water stress in the two studied DI treatments. Now, the seasonal course of DEp for the DI60 treatment showed no big differences in water consumption between the 60RDI tree and the control tree (Fig. 7A). This could be due to the great capacity of the olive tree to take up water from drying soils, reported by Dichio et al. (2003) and Cuevas et al. (2010), among others. The fact that the level of water stress imposed to the DI60 tree did not have a significant effect on its water consumption, may curtail the performance of the DMXTD approach for assessing crop water needs in commercial olive orchards. Our data shows that this disadvantage can be avoided by simultaneously recording both DEp and DMXTD which will inform on the effect of water stress on the tree’s water consumption. We have to be cautions with results shown in Figs. 6 and 7, because they have been derived from Q and TDV records in single trees. If further research with enough number of replicates renders similar results, we could concluded that the use of DEp and DMXTD values derived from simultaneous records of Q and TDV is an advantageous approach both to monitor water stress and to assess water needs in ‘Manzanilla’ olive trees with heavy fruit load. This approach, therefore, has a potential to be used for precise irrigation scheduling in commercial olive orchards.

5. Conclusions For old, big ‘Manzanilla’ olive trees with heavy fruit load growing in a soil with medium to high water holding capacity, the signal intensity approach for both Ep and MDS showed a poor reliability for detecting water stress in deficit irrigated trees. Knowledge

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on the physiological behaviour of the species must be taken into account for interpreting both the Q and TDV records, especially when sudden changes in atmospheric demand and soil water content occur, e.g. when recovery irrigations are applied. The time course of DMXTD was useful to indicate the onset, and severity, of water stress both in the DI60 and DI30 trees. The time course of DEp showed that the occurrence of water stress in the DI60 tree had little impact on its water consumption, as compared to that of the FI tree. Therefore, the simultaneous use of DMXTD and DEp increases the potential of Q and TDV records to assess water needs in mature olive orchards, as compared to the use of one method alone. Further research is needed to confirm these results and determine the optimum number of instrumented trees. Acknowledgements This work was funded by the IFAPA, Consejería de Innovación, Ciencia y Empresa de la Junta de Andalucía, research project ref. C03-056, and by the CICYT/FEDER, research projects AGL20040794-CO3-02/AGR and AGL2007-66279-CO3-02. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.envexpbot.2011.04.004. References ˇ Cermák, J., Kucera, J., Baurerle, W.L., Phillip, N., Hinckley, M., 2007. Tree water storage and its diurnal dynamics related to sap flow and changes in stem volume in old-growth Douglas-fir trees. Tree Physiol. 27, 181–198. Cohen, M., Goldhamer, D.A., Fereres, E., Girona, J., Mata, M., 2001. Assessment of peach tree responses to irrigation water deficits by continuous monitoring of trunk diameter changes. J. Hortic. Sci. Biotechnol. 76 (1), 55–60. Conejero, W., Alarcón, J.J., García-Orellana, Y., Abrisqueta, J.M., Torrecillas, A., 2007. Daily sap flow and maximum daily trunk shrinkage measurements for diagnosing water stress in early maturing peach trees during the post-harvest period. Tree Physiol. 27, 81–88. Connor, D.J., Fereres, E., 2005. The Physiology of adaptation and yield expression in olive. Hortic. Rev. 34, 155–229. Cuevas, M.V., Torres-Ruiz, J.M., Álvarez, R., Jiménez, M.D., Cuerva, J., Fernández, J.E., 2010. Usefulness of trunk diameter variations for irrigation scheduling in a mature olive tree orchard. Agric. Water Manage. 97, 1293–1302. Diaz-Espejo, A., Walcroft, A., Fernández, J.E., Hafidi, B., Palomo, M.J., Girón, I.F., 2006. Modelling photosynthesis in olive leaves under drought conditions. Tree Physiol. 26, 1445–1456. Dichio, B., Xiloyannis, C., Angelopoulos, K., Nuzzo, V., Bufo, A.S., Celano, G., 2003. Drought-induced variations of water relations parameters in Olea europaea. Plant Soil 257, 381–389. Drew, D.M., Downes, G.M., 2009. The use of precision dendrometers in research on daily stem size and wood property variation: a review. Dendrochronologia 27, 159–172. Fereres, E., Evans, R.G., 2006. Irrigation of fruit trees and vines: an introduction. Irrig. Sci. 24, 55–57. Fereres, E., Ruz, C., Castro, J., Gómez, J.A., Pastor, M., 1996. Recuperación del olivo después de una sequía extrema. In: Proc. of the XIV Congreso Nacional de Riegos. Aguadulce (Almería) , Spain, 11–13 June, pp. 89–93. Fernández, J.E., Cuevas, M.V., 2010. Irrigation scheduling from stem diameter variations: a review. Agric. For. Meteorol. 150, 135–151. Fernández, J.E., Moreno, F., 1999. Water use by the olive tree. J. Crop Prod. 2, 101–162. Fernández, J.E., Moreno, F., Cabrera, F., Arrúe, J.L., Martín-Aranda, J., 1991. Drip irrigation, soil characteristics and the root distribution and root activity of olive trees. Plant Soil 133, 239–251. Fernández, J.E., Moreno, F., Girón, I.F., Blázquez, O.M., 1997. Stomatal control of water use in olive tree leaves. Plant Soil 190, 179–192. Fernández, J.E., Palomo, M.J., Díaz-Espejo, A., Clothier, B.E., Green, S.R., Girón, I.F., Moreno, F., 2001. Heat-pulse measurements of sap flow in olives for automating irrigation: tests, root flow and diagnostics of water stress. Agric. Water Manage. 51, 99–123. Fernández, J.E., Palomo, M.J., Díaz-Espejo, A., Girón, I.F., 2003. Influence of partial soil wetting on water relation parameters of the olive tree. Agronomie 23, 545–552. Fernández, J.E., Diaz-Espejo, A., Infante, J.M., Durán, P., Palomo, M.J., Chamorro, V., Girón, I.F., Villagarcía, L., 2006a. Water relations and gas exchange in olive trees under regulated deficit irrigation and partial rootzone drying. Plant Soil 284, 271–287.

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