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Sap flow and daily electric potential variations in a tree trunk
Plant Science 171 (2006) 572–584 www.elsevier.com/locate/plantsci
Sap flow and daily electric potential variations in a tree trunk Dominique Gibert a,*, Jean-Louis Le Moue¨l c, Luc Lambs b, Florence Nicollin a, Fre´de´ric Perrier c,d a
Ge´osciences Rennes (CNRS UMR 6118), Universite´ Rennes 1, Baˆt. 15 Campus de Beaulieu, 35042 Rennes cedex, France b Laboratoire Dynamique de la Biodiversite´, CNRS, 29 rue Jeanne Marvig, 31055 Toulouse, France c ´ Equipe de Ge´omagne´tisme, Institut de Physique du Globe de Paris, 4 place Jussieu, 75252 Paris cedex 05, France d Commissariat a` l’e´nergie atomique, 91680 Bruye`res-le-Chaˆtel, France Received 11 January 2006; received in revised form 9 May 2006; accepted 2 June 2006 Available online 10 July 2006
Abstract Electric potential has been monitored since December 2003 in the roots and at two circumferences and one vertical profile in a standing poplar (Populus nigra). Electric potential is sampled using 6 mm diameter stainless steel rods, inserted 5 mm deep in the sapwood and is referenced to an unpolarisable lead/lead chloride electrode installed 80 cm deep in the soil. Diurnal variations are observed with seasonal differences. During winter, diurnal variations depend on the measurement point, with variable amplitudes and sometimes anti-correlations between electrodes. By contrast, a stable and coherent organisation is established in the spring, with larger amplitudes, and lasts during summer. Dedicated experiments have been performed to rule out a direct effect of temperature on the electrodes, and thus, demonstrate a genuine electrical source in the tree. Daily electrical variations have been reported previously, and have been interpreted as electrokinetic effects associated with sap flow. However, a comparison of the electrical signals with a direct measurement of the sap flow by a continuous heat flow method, shows that the electrical variation, although clearly correlated to sap flow, is not simply proportional to it. In a living system, electrokinetic effects, in addition to thermoelectrical effects, are probably modified significantly by additional electrochemical effects, such as membrane diffusion potentials, ion active transport by proteins or action potentials. Electric potential variations in trees may thus, reveal physical mechanisms in living systems not accessible by other methods. A better understanding of the electrical response of trees associated with sap flow may improve the knowledge of transfer processes between the soil and the atmosphere. This is important for the understanding of adaptive response of trees, the modelling of water and carbon balance in relation to climate change, and the quantification of the contribution of trees to the migration, retention and dispersion of contaminants. # 2006 Elsevier Ireland Ltd. All rights reserved. PACS: 02.70.Uu; 02.30.Zz; 91.25.Qi; 91.35.Pn; 91.40. k; 93.30.Vs Keywords: Electric potential; Electrokinetic effects; Membrane potential; Sap flow; Temperature effects
1. Introduction Estimating the effect of global climatic changes on ecosystems and the associated feedback mechanisms requires a better understanding of tree transpiration and carbon assimilation [1]. These processes depend on sap flow, which drives the whole tree physiology, the water balance and the hydrology of the subsurface as well (e.g., [2–5]) and they * Corresponding author. Tel.: +33 223236091; fax: +33 223236090. E-mail addresses: [email protected] (D. Gibert), [email protected] (J.-L. Le Moue¨l), [email protected] (L. Lambs), [email protected] (F. Nicollin), [email protected] (F. Perrier). 0168-9452/$ – see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2006.06.012
have been studied in dedicated large-scale field experiments (e.g., [6,7]). The direct measurement of sap flow up to now is based on thermal methods [8], which can be separated into heat pulse velocity techniques and heat balance techniques [9]. However, the calculation of the total water flux remains difficult. At the forest level, the water is shared between trees of different species and sizes [10]. At the tree level, several points need clarification, such as the contribution of night respiration [11,1], the radial variation of the sap velocity in the sapwood [12,13] or the occasional reverse sap flow in roots [14]. Sap flow is different for the three major xylem sap conducting systems (non-, diffuse- and ring-porous) and does not bear a simple relationship with tree diameter or canopy surface. Estimating the water flux from sap velocity
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measurement, thus, remains affected by large uncertainties [10]. Sap flow may also be accessed through measurements of the spontaneous electric potential of trees. Early measurements in an elm trunk [15] showed that the electric potential of the trunk with respect to a ground electrode shows daily variations with amplitude of the order of 20–40 mV, and a minimum of the potential in the afternoon. These daily variations have been associated with the sap flow. Indeed, the motion of liquids in porous media produces electric potential variations referred to as streaming potentials or electrokinetic effects (e.g., [16–20]). This effect is characterised by one coupling parameter, the streaming potential coefficient, defined as the ratio of the potential difference to the pressure difference. Electrokinetic effects have been observed in laboratory experiments with rocks (e.g., [21]); they lead to remarkable spatial and temporal variations of the spontaneous electric potential (SP) in natural conditions [22,17,23], especially near active volcanoes (e.g., [24]). The early observation on the tree trunk was confirmed by an experiment on a spruce tree [25], which in addition reported a non-linear relationship between the daily electric potential variation and the intensity of the solar radiation. Measurements at the surface of a chestnut tree [26] indicated that the time variations of the electric potential depend strongly on the season. In summer, clear daily variations of the trunk potential are observed, with a minimum in the afternoon when upper electrodes are referred to lower electrodes, in agreement with the previous experiments. In the late fall, after leaf shedding, these clear daily variations disappear, as expected if sap flow is the dominating mechanism for electric potential generation. However, electrical signals, with more erratic time variations, are still observed, indicating that other mechanisms may also contribute, possibly unrelated to sap flow. The electric potential was also monitored at several points of a Turkey oak (Quercus cerris) during 2 years [27,28]. This experiment indicated that the summer daily variations are in phase at the various points, with again a minimum of the potential with respect to the ground in the afternoon. The amplitude can vary by more than a factor of two from point to point. Two periods for large daily variations were observed: end of March and summer (end of June–July). Streaming potentials have also been studied in Salix alba L. sapwood samples in the laboratory and the results have been compared with the observed electrical daily variation in a standing tree to obtain estimates of the sap flow velocity [29]. The sap flow velocity, thus, estimated from the electrical variations, is 15–17 m h1, which is much higher than the accepted values for S. alba L., which are of the order of 2– 3 m h1[29]. The positive sign of the streaming potential coefficient obtained in the laboratory is in agreement with the sign reported for most rocks in usual natural conditions (e.g., [30]), but does not agree with the sign of the observed electric daily variation in the tree trunk. Indeed, for a positive streaming potential coefficient, the potential of the trunk should be positive with respect to the ground. While the observed daily variation could be reasonably interpreted at first in terms of streaming potentials, the relationship between the sap flow and
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the electric potential variation therefore remains puzzling. Other effects, such as thermo-electrical effects, membrane potential and experimental artifacts, need to be considered before a coherent physical interpretation can be proposed. It appears, therefore, interesting to undertake new experiments to investigate in more details the relationship between the sap flow and the electric potential variations in a tree. Monitoring of the electric potential in trees and more generally in living plants, may be interesting for other reasons. Electric activity has been evidenced in hibiscus and maize (e.g., [31,32]) and electrical signals have been observed in response to changes in transpiration and photosynthesis in willow plants [33] or Mimosa pudica [34]. The electric potential in trees may, therefore, reflect a combination of physical, chemical and physiological responses in relation with water transport, photosynthesis and adaptive feedback mechanisms. The seasonal variation of the electrical daily variation, for example, may be closely associated with the poorly understood seasonal variations of the enzymes of sucrose metabolism [35]. In this paper, we present a new experiment lasting more than 2 years in a poplar tree. In this experiment, we have focused on the spatial and temporal variations of the electric potential distribution in a single tree, using an increased number of electrodes compared with previous work. The comparison of several trees will be considered in a later stage. The experimental set-up is first presented. After a brief overview of the annual cycles of the tree, we present specific experiments performed to constrain the physical mechanisms. In particular, the electrical daily variations are compared with a direct and independent measurement of the sap flow with a thermal method. In addition, temperature effects, which can potentially affect the measured electric potential, are studied in details. In the conclusion, we discuss the generation mechanisms of electric potential in the tree trunk. 2. Experimental set-up 2.1. Electrode array The investigated tree is a poplar (Populus nigra L.) located in Remungol1 (Brittany, France). The first part of the experimental set-up, with a set of 26 electrodes, was installed on August 6, 2002, 21 electrodes in the trunk and five in two emerging roots (Figs. 1 and 2). Trunk electrodes are arranged in three groups: two circular rings and one vertical line. The lower ring, with eight electrodes numbered E1 to E8, is located 1.0 m above the ground and has a circumference of 2.7 m. The upper ring, with eight electrodes numbered E11 to E18, is located 3.4 m above the ground and has a circumference of 2.4 m. The vertical line comprises five electrodes numbered from E30 (0.5 m above the ground) to E34 (2.9 m above the ground) and aligned with E6 and E16 on the northern face of the trunk. Root electrodes E01, E02 and E03 (Figs. 1 and 2) are implanted in a root running 1 WGS 84 geographic coordinates: 47 560 0500 N and 2 530 4500 W, i.e. Universal Time used in figures is almost the same as the local Solar Time.
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Fig. 2. Plan view showing the canopy area, the trunk and the two roots equipped with electrodes. Also shown are the two Petiau electrodes, P1 and P2.
Fig. 1. General view (from west) of the array of electrodes shown as black dots on a simplified sketch of the tree. The box labelled T–H indicates the position of the outdoor temperature and humidity sensors.
eastward from the trunk, partially emerging from the ground. The diameter of this root is about 0.18 m, and the electrodes E01, E02 and E03 are at distances of 0.45, 0.90 and 1.35 m from the eastern edge of the trunk, respectively. Electrodes E04 and E05 are located at 0.6 and 1.2 m from the north-eastern basis of the trunk on a shallow root with a diameter of 0.15 m (Fig. 2). Seven electrodes (E21 installed on May 31, 2003, and E22 to E27 installed on August 18 and 27, 2004) were added along a vertical segment whose lower (E21) and upper (E26 and E27) ends are at 5.6 and 10.5 m above the ground, respectively (Fig. 1).
The electrodes have a diameter of 6 mm and were cut in stainless steel rods which were carefully degreased 1 day before the installation. The apparent metallic part of the electrodes is cut to 15 mm, and each electrode is connected by wrapping a cable which is secured with a epoxied cap of thermo-sheath (Fig. 3). The connectivity of an electrode with its cable is tested with an ohm-meter. The electrodes are inserted in the tree by drilling a hole with a diameter of 8 mm through the bark and another one with a diameter of 6 mm and a depth of 15 mm in the wood. Next, the electrodes are gently hammered until being embedded in the wood. In this way, the non-isolated metallic part of the electrodes is fully stuck in the wood so that the meteorological influences, such as rain or fast temperature changes are reduced. The contact resistance of the electrodes has been measured with an AC ohm-meter and varies from 4700 to 6400 V with an average of 5400 V. The electrode array is complemented with a nonpolarisable lead–lead chloride electrode [36] which is used as a reference for all potential measurements. This electrode is located 5.0 m away from the tree in the eastward direction (Figs. 1 and 2) and is buried at a depth of 0.7 m with clay as contact material. On May 31, 2003, another nonpolarisable electrode labelled E102, was buried using the same method at a depth of about 0.3 m near the root electrode E01. 2.2. Data acquisition system Data acquired at the beginning of the experiment are not used in the present study, and only those obtained with the digital acquisition system installed in November 2003 are presented here. The measurement device is a Keithley 2701 digital multimeter with an input impedance larger than 100 M V and equipped with a relay matrix having 40 measurement
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Fig. 3. Top: detailed view of an electrode. The apparent metallic part of the electrode is fully embedded in the wood. The epoxied cap secures the cable which is wrapped around the stainless steel rod. Bottom left: view of an electrode placed on the tree. The uncovered part of the electrode is fully embedded in the wood under the bark in order to reduce meteorological influences. Bottom right: in the Granier’s method, the sap flux is obtained by measuring the thermal flux advected by the sap flow with one heater (H) and two thermo-couples (T).
channels controlled through an acquisition software. Measurements of the electric potential are made at all electrodes with a sampling interval of 1 min. We use a UT time base, synchronised in real time to the Frankfurt atomic clock. Both the computer and the multimeter are powered with a backup generator which prevents breaks caused by short failures of the electrical power line. In order to check the entire electrical system, and in particular, the high input impedance of the recorder, we performed several injections of electrical current in the soil near the basis of the tree. The applied voltage at the grounded electrodes was 12 V for an electrical current of 2.5 mA. Fig. 4 shows the electrical potential measured at several
electrodes during two current injections of opposite signs. The response due to the injections is clearly seen on all channels. In addition, the electric potential response happens within one sampling time. This indicates that our measurements are not affected by artificial delay times or capacitive effects, that could, for example, have resulted from an insufficient input impedance of the acquisition system. Such tests are performed regularly. 2.3. Meteorological measurements In November 2003, a meteorological station was installed to record the main atmospheric parameters in the neighbourhood of the tree. The measured parameters include the speed and direction of the wind, the atmospheric pressure, the outside temperature and humidity, the rain events. Temperature and humidity are also measured indoor in order to identify a possible sensitivity of the electronic devices to the environmental conditions. All meteorological parameters are recorded every 15 min and synchronised with the time base used for the potential measurements. 2.4. Influence of temperature on the electrode array
Fig. 4. Electrical potential measured at several electrodes during an injection of electrical current in the soil near the tree. Hours are given in Universal Time.
Stainless-steel electrodes might be affected by significant temperature effects, and it is important to discuss purely thermal effects as the cause of the observed diurnal variations of the electric potential. In principle, this is possible, as the temperature sensitivity of the electrode–wood contact may be a
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present in the curve of the outdoor temperature measured in the vicinity of the tree (Fig. 1). This condition is, however, not due to a temperature effect at the electrodes, but to a global effect affecting the whole tree. This was further checked by studying the correlation between the potential and temperature curves. In particular, we observed that the correlation between the E6 and E31 potential curves is maximal for zero-time delay both before and, significantly, after the installation of the insulating pot on E31. Conversely, when the pot is installed, the correlation between the outdoor and E31 temperature curves is maximum for a time-delay of 45 min. This is another manner to demonstrate that the delayed correlation between electric potential and outdoor temperature results from the activity of the tree. 2.5. Sap flow measurements
Fig. 5. Thermal tests made on electrode E31 to verify that no important potential variations are induced by temperature. Potential at nearby E6 electrode and outdoor temperature are given for reference. The transient variations of E31’s potential are observed when introducing the warm (or cold) bottle in the box covering the electrode. Hours are given in Universal Time.
rapidly varying function of the water content in the wood and the air humidity. Temperature influence on the tree electrodes would introduce temporal effects depending on position. For instance, the amplitude of the potential variations should be larger on the south side exposed to solar heating. Note that this is not what we observe actually; however, dedicated thermal experiments were performed to check for a possible temperature effect on our electrode array. As shown by Petiau [36], the temperature sensitivity of the grounded electrochemical electrode used as as reference is negligible (smaller than 30 mV= C), and our thermal experiment focused on the steel electrodes. In August 2004, we applied large artificial thermal perturbations to E31 which was previously covered with an insulating pot. Fig. 5 shows the results obtained during both a heating and a cooling test done by introducing a bottle of hot water or ice in the pot. Excepted for sharp transient variations of the potential occurring when introducing the bottle, no perturbation of the E31 potential is observed when compared with the potential measured on the nearby E6 electrode. This clearly rules out a direct effect of temperature on the measured electrode potential. Looking at Fig. 5 more closely, we observe that potential variations at both E31 and E6 have features similar to those
During a limited period of time (from June 21 to July 15 of 2004), direct measurements were performed in addition to the electrode measurements. The sap flow is measured with the heat-balance technique initially proposed by Granier [9]. This method uses a pair of probes, each equipped with a small resistor to produce heat and a miniature thermocouple to measure the temperature inside the wood. The diameter of a probe equals 2 mm for a length of 20 mm. Only the upper heater is turned on and both probes are used to make differential temperature measurements in order to measure the thermal imbalance due to sap flow (Fig. 3). One pair of probes was placed in the root near E01 and two pairs were placed 10 cm apart between E31 and E32 (Fig. 1). The part of the trunk holding the probes was covered with an insulating blanket in order to attenuate the thermal perturbations produced by the atmospheric variable conditions. The temperature was measured every 5 min and these data were later converted into sap flow current through an experimentally derived calibration [9]. 3. Presentation of data 3.1. Overview of electric potential variations Figs. 6–9 present the data for seven electrodes from December 1, 2003 to May 21, 2005. This choice of seven electrodes is representative of the whole electrode array: one root electrode (E01), E6 on the lower ring, E11 and E18 on the upper ring, E34 located on the vertical line just beneath the upper ring, E21 and, when available, E25 located on the vertical line 5.50 and 9.50 m above the floor, respectively. Two breakdowns of long duration interrupt the curves, the first from January 12, 2004 to February 17, 2004, the second from September 4, 2004 to September 15, 2004. These recordings of long duration show that the electrical activity is present on all electrodes over the whole time span although with varying amplitudes and a high variability from one electrode to another. Large daily variations are present on most electrodes from spring to summer. A first important observation is the persistence of the electrical activity during
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Fig. 6. Top: potential signals measured on six electrodes representative of the entire electrode array for the December 2003–April 2004 period. Relative potential values. Bottom: outdoor temperature measured near the tree (see Fig. 1 for location). Tick marks fall at midday.
Fig. 7. Same as Fig. 6 for the April–August 2004 period.
Fig. 8. Same as Fig. 6 for the September 2004–January 2005 period.
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Fig. 9. Same as Fig. 6 for the January–May 2005 period.
winter (Figs. 6 and 8) when the tree activity is expected to be greatly reduced. During this period, a daily variation is observed on all electrodes, sometimes with a high amplitude as large as the one seen in spring and summer. This is, for example, the case for electrode E18 whose diurnal amplitude remains of the order of 30–50 mV all year long. Note that in December, the E6 curve appears to be the upper envelope of the E18 signal. In winter, the signals appear one-sided with daily positive jumps with respect to a smoothly varying base level. In spring and summer, this one-sided structure is less visible and replaced by a more symmetrical pattern. This is particularly clear when comparing the E18 curve in September and December 2004 in Fig. 8. At many points in the tree, long-term and daily electric potential variations appear anti-correlated with the variations of the outdoor temperature. This is, for example, the case for the long-term trends of E01 and E6 in December 2003 (Fig. 6), or for the long-term trend and the daily variations of E6 March– April 2004. Note, however, that in March–April 2004, there is no clear relationship between E01 and the temperature,
indicating that this anti-correlation between electric potential and temperature is complex and time-dependent. When considering the diurnal signal of a given electrode on a long-term basis (Figs. 6–9), larger temperature daily variations are not systematically associated with larger electrical diurnal amplitudes as would be expected for a dominant temperature effect. These observations, together with the thermal tests discussed above, rule out the hypothesis that the observed electrical variations are due to a purely thermal artifact at the electrical contact between steel and wood. Instead, a physical mechanism indirectly connected to the temperature and involving the activity of the tree must be invoked, as proposed by previous authors. Additional peculiar observations are made when looking at the period from February to March 2004, a period which is also shown with an enlarged time scale in Fig. 10. During this period, all electrodes, except electrode E18, display large negative peaks, for example, around February 23, March 7 or March 13 (Fig. 10), while E18 shows a more regular daily variation. Interestingly, these large negative peaks on the
Fig. 10. Enlargement of a part of Fig. 9 showing the occurrence of negative daily jumps of the electric potential (E6, E34, E11 and E21) corresponding to negative outdoor temperature. Notice the persistence of the daily positive jumps for electrode E18. Tick marks of horizontal axis fall at midday.
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Fig. 11. (a) Sap flow measured with two probes located near E32. (b) Outdoor temperature. (c) Electrical potential measured at E32. (d) First time-derivative of the E32 potential shown in (c). Tick marks of horizontal axis fall at midday.
potential occur precisely when the temperature goes below zero. The same phenomenon is observed during the winter of 2004–2005 (Fig. 9), especially in the second half of February 2005. The zoomed signals shown in Fig. 10, reveal the occurrence of dipolar transient signal with a duration of several hours on March 3 and 6, 2004. Such signals frequently occur with a duration varying from several minutes to several hours. The amplitude of the dipolar signal increases with the altitude of the considered electrode, a feature observed for all similar signals we examined, which rules out the possibility that these signals are caused by instabilities of the reference ground electrode. The amplitude of these transient signals depends more strongly on altitude than observed for the step-like signals recorded during the test of current injection in the soil (Fig. 4). It is then unlikely to explain these transient signals by invoking telluric currents, either natural or anthropic, originating from the ground. Rain or storms, which could have been a first explanation, must also be excluded using our meteorological data. The origin of such signals, which appear occasionally, remains unclear and deserve further study. A big change occurs in the recorded signal from winter to spring in both years 2004 and 2005 with the onset of a stable daily activity at all electrodes. This onset is particularly clear in April and May of years 2004 (Fig. 7) and 2005 (Fig. 9) with starting times differing of several weeks from one electrode to another. For instance, activity begins around March 20, 2005 for E18 and around May 1, for E25 (Fig. 9). Once established, the daily activity remains high during summer and autumn, and the return to the low winter activity also occurs at noticeably different dates depending on the electrode (Fig. 8). 3.2. Comparison with sap flow measurements We now turn to the comparison between electrical signals and sap flow measurements. The sap flow curves corresponding
to the probes located near E32 are shown in Fig. 11 a for the period going from June 21 to July 15, 2004. The two curves show clear diurnal variations; they have a similar appearance but their amplitudes differ up to a factor of two on certain days. The electrical potential (Fig. 11c) measured at E32 and its first time-derivative (Fig. 11d) also show a diurnal variation with a variable amplitude which does not appear to be directly related to the amplitude of the sap flow. The same temporal variation of the electrical signal was observed during the days preceding the installation of both the thermal probes and the insulating blanket. This ensures that the electrical variations are not due to the heating device. To look more closely at the correlation between the electrical signal and the sap flow, a period of 4 days was selected (Fig. 12). This detailed view allows to examine precisely the temporal coincidence between the sap flow and the electrical variations, either in the potential curve or in its time-derivative. The variations goes from the early time in the morning, when the sap flow begins to be reactivated, to the mid-morning when the sap flow reaches its maximum value. During this period of sap flow reactivation, the timederivative of the potential curve shows a conspicuous bipolar variation with a high amplitude, beginning with a positive lobe. The late negative lobe of the bipolar event reaches its minimum value (black dashed line) precisely when the sap flow stops increasing and reaches a plateau. At that time, the potential begins to decrease and becomes minimal slightly after the sap flow has left its plateau-level and begins to diminish sharply. The electrical potential then returns to its original value in about 8 h, while a zero sap flow is reached faster, after about 4 h. The time when zero sap flow is reached (red dashed line) or keeps decreasing slowly asymptotically to zero, also coincides approximately with the maximum of the time-derivative of the electrical potential. Notice that a large electrical signal still remains while the sap flow has completely vanished.
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Fig. 12. Same as in Fig. 11 for a limited period showing the correlations between electrical and sap flow events. Hours are given in Universal Time.
electrodes. Our new observations make this interpretation quite questionable. Indeed:
4. Discussion In the rather small number of experiments made on standing trees, listed in the introduction, the measured electric potentials were attributed to an electrokinetic effect forced by the sap flow [15,26,25]. The rough agreement of the value of the electrokinetic coupling coefficient measured in the laboratory with the value required to account for the observed magnitude of the potentials in the standing tree was taken as a strong clue in favour of this hypothesis, although the sign does not appear to be the correct one. Furthermore, these previous experiments were generally performed over short time periods, with few
(1) A negative potential is observed on all the trunk electrodes with respect to the ground. (2) In the framework of electrokinetic theory, the electric field is proportional to the pressure gradient, hence, to the sap flow per unit surface. This implies, at least in average, for example, taken over the eight electrodes of a ring, a linear increase of the electric potential amplitude with height in the trunk (recall that the reference electrode is located in the ground). This variation is not observed at all (Fig. 13).
Fig. 13. Amplitude of the electric potential variation from the 5:00 a.m. to 5:00 p.m. period of June 1, 2004.
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(3) The heterogeneity of the diurnal amplitudes of the electric potential from electrode to electrode is difficult to explain in terms of an electrokinetic effect. Of course, we may expect lateral heterogeneity in the xylem vessels through which the sap is pumped up. However, the tree is a conducting medium, and some homogenisation of the potential at a given height is expected. (4) The strongest argument comes from the comparison of the electric potential curves with the sap flow curves (Figs. 11 and 12). Clearly, the electric potential is not at pace with the sap flux, assuming that the thermal method measures the sap flux with negligible retardation. Actually, our measurements of the sap flow at two different points provide the same time variation and support this assumption. In particular, we note that a strong negative potential is still present after the sap flow has receded, around 10 p.m. (Fig. 12); it is at this very moment that the curve of the time-derivative of the potential reaches its maximum value. Similarly, in the morning, during the 2-h time interval taken by the sap flux to reach its maximum, the electric potential hardly changes. These observations cannot be reconciled with the electrokinetic mechanism in its simple form. (5) The electric potentials in a root and in the nearby soil are not equal (Fig. 14), suggesting the presence of an electrical barrier between the tree root system and the soil. Nevertheless, the curves of Figs. 11 and 12 evidence a stable functional relationship between the sap flow and the electric potential. To simplify the picture, it appears that the sap flow polarises (electrifies) negatively the whole tree trunk with respect to the ground; but this polarisation process has a long time constant, on the order of hours; when the sap flow vanishes, in the evening, it is with this long time constant that the polarisation also goes to zero. Another remarkable fact is that the rapid onset of the sap flux in the morning generates a specific transient variation on the electric potential, particularly outstanding in its time-derivative (Fig. 12).
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A well known phenomenon in geophysical prospecting, although still poorly understood, is the so-called induced polarisation (e.g., [37,38]). Injecting electric current into the ground through two electrodes generates an electric field in their neighbourhood; when switching off the current source, the potential goes back to zero with a time constant which can sometimes reach several seconds, depending on the nature of the ground and of the electrodes (e.g., [39,37]). Such induced polarisation effects can be particularly strong in the presence of ore deposits, which is the basis of its use as an empirical prospecting method. This observation reveals the ubiquitous presence of electromotive forces in the ground after turning off the external current source. In their absence, the ground would be back instantaneously equipotential. However, the time constant involved in the present experiment is so large that it seems necessary to call for a mechanism specific to biological living systems. Note that all the curves corresponding to the different electrodes behave in a similar fashion with respect to the sap flow curve, while the amplitudes of this daily variation differ greatly from point to point. This time constant does not appear specific to a given neighbourhood but characterises the whole tree. The mechanism that could be invoked to generate such a trunk polarisation and time constant remains unclear. As mentioned in the introduction, the observed electric potential may reflect a combination of physical, chemical and physiological responses to the sap flow, photosynthesis and adaptive feedback controls of the tree. While we are not able to propose a comprehensive model at this stage, we can sketch the following scenario. We have to find a mechanism able to accommodate the peculiar electrical system observed in the tree trunk. The trunk is a conductor, but the electrical potential, which depends on the position vector r and time t, must be able to sustain a temporal relaxation of the form: @Vðr; tÞ Vðr; tÞ þ ¼ F½r; SðtÞ; @t t
(1)
Fig. 14. Example of diurnal potential variation measured on a chemical electrode (E102) placed in the soil near the root electrode E01. Note the different vertical scales used for both potential curves (left scale for E01 and right scale for E102). Major tick marks of horizontal axis fall at midday.
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Fig. 15. (a) Main electrical structure of a sectional cross-section of the tree trunk. Small longitudinal capacitive elements are composed by insulating xylem elements embedded in the conductive trunk and containing the circulating and conducting sap (b).
where t is some relaxation time and F is some positiondependent functional of the sap flow SðtÞ, vanishing when the sap flow vanishes. As t is of the order of several hours, some poorly conducting medium must be present within the conductor, able to generate a significant capacitance. In addition, we know that F is a negative function of S, basically constant with height z, but smoothly varying around the circumference. This imposes a configuration of the source with translational symmetry along the tree axis, as depicted in Fig. 15 a. The spatial configuration of the potential results from leakage of charge accumulated within this supposed nonperfect isolator. Note that a grounded perfect conductor with an inner distribution of charge is characterised by constant potential and spatially varying surface charge distribution. Here, we have a non-perfect insulator embedded in a non-perfect conductor, which allows to maintain a small volume current. As the potential varies with azimuth, we have to conclude that the charge distribution maintained by the insulator is not
cylindrical. This probably requires a non-cylindrical sap flow as well. In our tree, given the asymmetric distribution of branches and roots around the axis of the trunk (Fig. 2), it may not be unexpected. Note that the two measurements of sap flow also support a non-cylindrical sap velocity. At each electrode, the potential is the result of the potential distribution due to sum of all the individual electrical sources, namely the leakage of all the supposed elementary capacitors (Fig. 15). Once this electrical mechanism is proposed, the role of the sap flow can be sketched as follows. Let us consider a xylem element (Fig. 15b). The conducting sap pervades the trunk and makes it a conductor; when photosynthesis and transpiration are active, it is circulating upwards in xylem elements. The walls of such elements are made of insulating ligneous cell walls. In the case of a solid rock surface, elementary charges are adsorbed, creating an excess charge in the electrolyte. It is the motion of this excess charge that creates the electrokinetic effect. In our case, however, a different situation happens, which completely changes the resulting distribution of currents. Indeed, imagine that the electric charges are not just adsorbed at the solid surface, but are now allowed to freely diffuse within the wall. What now dominates the electrical current is not the circulation along the axis of the trunk but the radial charge transfer. When the sap flow is suppressed, the charge carriers slowly diffuse back to the sap electrolyte or alternatively may get neutralised within the wall. This situation is analogous to a heat source in an underground cavity [40]. The temperature in the cavity during heating is rising linearly after some time, corresponding to a steady state heat transfer from the cavity to the surrounding rock. When the heat source is removed, the temperature is going back to the initial state, but with a dynamics controlled by the diffusion of heat in the walls. If this analogy is relevant for the tree potential, then the relaxation should actually not be exponential but a power law of time. The data in the tree at this time do not allow to distinguish between the two different types of relaxation. To summarise, we propose that the spatio-temporal characteristics of electrical potential in the tree trunk might be explained by a biological mechanism allowing the diffusion of charge carriers (e.g., heavy protein fragments or charge carrying hormones) across the insulating gel of the xylem walls. Maybe this charge transport is controlled actively by dedicated ionic channels in the wall, followed by molecular diffusion once across the membrane. Such a mechanism then suggests the presence of electrically active structures within the xylem channels. Thus, the xylem may play a more active role in the electrical response than would have been expected from nonliving cells with pure conduction. 5. Conclusion This experiment confirms the existence and largely extends the investigation of specific daily variations of the electric potential distribution in a tree trunk as mentioned in previous studies [15,26–28]. These daily variations bear a definite relation to the simultaneously sap flow in summer. The
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observations of electrical variations in winter would then imply a sporadically varying sap flow, both in space and time, during this season. These results, deduced from measurements on a single tree, should be confirmed by performing analogous studies on several trees in order to get a statistical significance. While the order of magnitude of the observed variation is the same as observed by previous workers, an electrokinetic mechanism seems to be unable to account for the independence of the potential with respect to altitude. Instead, we propose a different mechanism based on charge diffusion from the conductive sap flow channels into the resistive xylem walls. This mechanism could be clarified by a dedicated experimental program, for instance, by performing measurements on small trees in the laboratory or by using ion-selective microelectrodes or energy dispersive X-ray microanalysis. Thus, electrical monitoring of a living tree can reveal both unexpected patterns of the sap flow and new mechanisms of charge exchange in xylem elements. These results should raise a renewed interest in electrical measurements in trees. Experiments with long-term monitoring using a large number of distributed electrodes are needed to make progress. Acknowledgments The authors thank Fre´de´ric Conil for technical assistance and Pierre Morat for guidance. This work is IPGP contribution no. 2149. We thank M.L. Gicquel for providing us with facilities during the experiment. This work was financially supported by the CNRS and ANDRA through the GdR FORPRO and corresponds to the GdR FORPRO contribution number 2006/03 A. References [1] S. Lebaude, N. Le Goff, J.-M. Ottorini, A. Granier, Carbon balance and tree growth in a Fagus sylvatica stand, Ann. For. Sci. 57 (2000) 49–61. [2] L. Lambs, M. Berthelot, Monitoring of water from the underground of the tree: first results with a new sap extractor on a riparian woodland, Plant Soil 241 (2002) 197–207. [3] L. Lambs, J.-P. Loudes, M. Berthelot, The use of the stable oxygen isotope (18O) to trace the distribution and uptake of water in riparian woodlands, Nukleonika 47 (2002) 115–155. [4] J.D. Johnson, R. Tognetti, P. Paris, Water relations and gas exchange in poplar and willow under water stress and elevated atmospheric CO2, Physiol. Plant. 115 (2002) 93–100. [5] L. Meiresonne, N. Nadezhdin, J. Cermak, J. Van Slycken, R. Ceulemans, Agric. Forest Meteorol. 96 (1999) 165–179. [6] A. Granier, P. Biron, D. Lemoine, Water balance, transpiration and canopy conductance in two beech stands, Agric. Forest Meteorol. 100 (2000) 291– 308. [7] L. Lambs, E. Muller, Sap flow and water transfer in the Garonne river riparian woodland, France: first results on poplar and willow, Ann. For. Sci. 59 (2002) 301–315. [8] R.H. Swanson, Significant historical developments in thermal methods for measuring sap flow in trees, Agric. Forest Meteorol. 72 (1994) 113–132. [9] A. Granier, Mesure du flux de se`ve brute dans le tronc du Douglas par une nouvelle me´thode thermique, Ann. Sci. For. 44 (1987) 1–14. [10] A. Guevara-Escobar, W.R.N. Edwards, R.H. Morton, P.D. Kemp, A.D. Mackay, Tree water use and rainfall partitioning in a mature poplarpasture system, Tree Physiol. 20 (2000) 97–106. [11] R. Benyon, Nighttime water use in an irrigated, Eucalyptus grandis plantation, Tree Physiol. 19 (1999) 853–859.
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[12] N. Phillips, R. Oren, R. Zimmermann, Radial patterns of xylem sap flow in non-, diffuse- and ring-porous tree species, Plant Cell Environ. 19 (1996) 983–990. [13] S.D. Wullschleger, A.W. King, Radial variation in sap velocity as a function of stem diameter and sapwood thickness in yellow-poplar trees, Tree Physiol. 20 (2000) 511–518. [14] S.S.O. Burgess, M.A. Adams, T.M. Bleby, Measurement of sap flow in roots of woody plants: a commentary, Tree Physiol. 20 (2000) 909–913. [15] D.S. Fensom, The bioelectric potentials of plants and their functional significance: V. Some daily and seasonal changes in the electrical potential and resistance of living trees, Can. J. Bot. 41 (1963) 831–851. [16] J.J. Bikerman, Electrokinetic potentials, in: C.A. Hampel (Ed.), The Encyclopedia of Electrochemistry, Reinhold Publishing Corporation, New York, 1964, pp. 471–475. [17] J.L. Thony, P. Morat, G. Vachaud, J.-L. Le Moue¨l, Field characterization of the relationship between electrical potential gradients and soil water flux, C.R. Acad. Sci. Paris 325 (1997) 317–321. [18] A. Revil, H. Schwaeger, L.M. Cathles, P.D. Manhardt III, Streaming potential in porous media 2. Theory and application to geothermal systems, J. Geophys. Res. 104 (1999), 20,033–20,048. [19] S. Marino, D. Coelho, S. Bekri, P.M. Adler, Electro-osmotic phenomena in fractures, J. Colloid Interface Sci. 223 (2000) 292–304. [20] F. Perrier, P. Morat, Characterization of electrical daily variations induced by capillary flow in the non-saturated zone, Pure Appl. Geophys. 157 (2000) 785–810. [21] V.A. Bogoslovsky, A.A. Ogilvy, The study of streaming potentials on fissured media models, Geophys. Prospect. 20 (1972) 109–117. [22] V.A. Bogoslovsky, A.A. Ogilvy, Natural potential anomalies as a quantitative index of the rate of seepage from water reservoirs, Geophys. Prospect. 18 (1970) 261–268. [23] M. Trique, F. Perrier, T. Froidefond, J.-P. Avouac, S. Hautot, Fluid flow near reservoir lakes inferred from the spatial and temporal analysis of the electric potential, J. Geophys. Res. 107 (B10) (2002) 2239, 10.1029/ 2001JB000482. [24] J. Zlotnicki, J.L. Le Moue¨l, Possible electrokinetic origin of large magnetic variations at La Fournaise Volcano, Nature 343 (1990) 633–636. [25] M. Schuch, R. Wanke, Die zeitlichen Variationen der electrischen Stro¨mungs-spannung in einem Fichtenstamm, verursacht durch die ta¨gliche a¨nderung des Saftstromes, Oecol. Planta 3 (1968) 169–176. [26] P. Morat, J.-L. Le Moue¨l, A. Granier, Electrical potential on a tree. A measurement of the sap flow? C.R. Acad. Sci. Paris 317 (1994) 98–101. [27] A. Koppa´n, L. Szarka, V. Wesztergom, Annual fluctuation in amplitudes of daily variations of electrical signals measured in the trunk of a standing tree, C.R. Acad. Sci. Paris 323 (2000) 559–563. [28] A. Koppa´n, A. Fenyvesi, L. Szarka, V. Wesztergom, Measurement of electric potential difference on trees, Acta Biol. Szegediensis 46 (2002) 37–38. [29] W. Gindl, H.G. Lo¨ppert, R. Wimmer, Relationship between streaming potential and sap velocity in Salix Alba L, Phyton 39 (1999) 217–224. [30] B. Lorne, F. Perrier, J.-P. Avouac, Streaming potential measurements, I: Properties of the electrical double layer from crushed rock samples, J. Geophys. Res. 104 (B8) (1999), 17, 857–17, 877. [31] J. Fromm, M. Hajirezaei, I. Wilke, The biochemical response of electrical signaling in the reproductive system of Hibiscus plants, Plant Physiol. 109 (1995) 375–384. [32] J. Fromm, H. Fei, Electrical signaling and gas exchange in maize plants of drying soil, Plant Sci. 132 (1998) 203–213. [33] J. Fromm, W. Eschrich, Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis, J. Plant Physiol. 141 (1993) 673–680. [34] C. Koziolek, T.E.E. Grals, U. Schreiber, R. Matyssek, J. Fromm, Transient knockout of photosynthesis mediated by electrical signals, New Phytol. 161 (2003) 715–722. [35] S. Schrader, J.J. Sauter, Seasonal changes of sucrose-phosphate synthase and sucrose synthase activities in poplar wood (populus canadensis Moench ‘‘robusta’’) and their possible role in carbohydrate metabolism, J. Plant Physiol. 159 (2002) 833–843. [36] G. Petiau, Second generation of lead-lead chloride electrodes for geophysical applications, Pure Appl. Geophys. 157 (2000) 357–382.
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[39] C. Schlumberger, E´tude sur la prospection e´lectrique du sous-sol, Gauthier-Villar, Paris, 1920. [40] C. Crouzeix, J.-L. Le Moue¨l, F. Perrier, P. Richon, P. Morat, Long term thermal evolution and effect of low power heating in an underground quarry, C.R. Acad. Sci. Geosci. Paris 335 (2003) 345–354.
Sap flow and daily electric potential variations in a tree trunk Dominique Gibert a,*, Jean-Louis Le Moue¨l c, Luc Lambs b, Florence Nicollin a, Fre´de´ric Perrier c,d a
Ge´osciences Rennes (CNRS UMR 6118), Universite´ Rennes 1, Baˆt. 15 Campus de Beaulieu, 35042 Rennes cedex, France b Laboratoire Dynamique de la Biodiversite´, CNRS, 29 rue Jeanne Marvig, 31055 Toulouse, France c ´ Equipe de Ge´omagne´tisme, Institut de Physique du Globe de Paris, 4 place Jussieu, 75252 Paris cedex 05, France d Commissariat a` l’e´nergie atomique, 91680 Bruye`res-le-Chaˆtel, France Received 11 January 2006; received in revised form 9 May 2006; accepted 2 June 2006 Available online 10 July 2006
Abstract Electric potential has been monitored since December 2003 in the roots and at two circumferences and one vertical profile in a standing poplar (Populus nigra). Electric potential is sampled using 6 mm diameter stainless steel rods, inserted 5 mm deep in the sapwood and is referenced to an unpolarisable lead/lead chloride electrode installed 80 cm deep in the soil. Diurnal variations are observed with seasonal differences. During winter, diurnal variations depend on the measurement point, with variable amplitudes and sometimes anti-correlations between electrodes. By contrast, a stable and coherent organisation is established in the spring, with larger amplitudes, and lasts during summer. Dedicated experiments have been performed to rule out a direct effect of temperature on the electrodes, and thus, demonstrate a genuine electrical source in the tree. Daily electrical variations have been reported previously, and have been interpreted as electrokinetic effects associated with sap flow. However, a comparison of the electrical signals with a direct measurement of the sap flow by a continuous heat flow method, shows that the electrical variation, although clearly correlated to sap flow, is not simply proportional to it. In a living system, electrokinetic effects, in addition to thermoelectrical effects, are probably modified significantly by additional electrochemical effects, such as membrane diffusion potentials, ion active transport by proteins or action potentials. Electric potential variations in trees may thus, reveal physical mechanisms in living systems not accessible by other methods. A better understanding of the electrical response of trees associated with sap flow may improve the knowledge of transfer processes between the soil and the atmosphere. This is important for the understanding of adaptive response of trees, the modelling of water and carbon balance in relation to climate change, and the quantification of the contribution of trees to the migration, retention and dispersion of contaminants. # 2006 Elsevier Ireland Ltd. All rights reserved. PACS: 02.70.Uu; 02.30.Zz; 91.25.Qi; 91.35.Pn; 91.40. k; 93.30.Vs Keywords: Electric potential; Electrokinetic effects; Membrane potential; Sap flow; Temperature effects
1. Introduction Estimating the effect of global climatic changes on ecosystems and the associated feedback mechanisms requires a better understanding of tree transpiration and carbon assimilation [1]. These processes depend on sap flow, which drives the whole tree physiology, the water balance and the hydrology of the subsurface as well (e.g., [2–5]) and they * Corresponding author. Tel.: +33 223236091; fax: +33 223236090. E-mail addresses: [email protected] (D. Gibert), [email protected] (J.-L. Le Moue¨l), [email protected] (L. Lambs), [email protected] (F. Nicollin), [email protected] (F. Perrier). 0168-9452/$ – see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2006.06.012
have been studied in dedicated large-scale field experiments (e.g., [6,7]). The direct measurement of sap flow up to now is based on thermal methods [8], which can be separated into heat pulse velocity techniques and heat balance techniques [9]. However, the calculation of the total water flux remains difficult. At the forest level, the water is shared between trees of different species and sizes [10]. At the tree level, several points need clarification, such as the contribution of night respiration [11,1], the radial variation of the sap velocity in the sapwood [12,13] or the occasional reverse sap flow in roots [14]. Sap flow is different for the three major xylem sap conducting systems (non-, diffuse- and ring-porous) and does not bear a simple relationship with tree diameter or canopy surface. Estimating the water flux from sap velocity
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measurement, thus, remains affected by large uncertainties [10]. Sap flow may also be accessed through measurements of the spontaneous electric potential of trees. Early measurements in an elm trunk [15] showed that the electric potential of the trunk with respect to a ground electrode shows daily variations with amplitude of the order of 20–40 mV, and a minimum of the potential in the afternoon. These daily variations have been associated with the sap flow. Indeed, the motion of liquids in porous media produces electric potential variations referred to as streaming potentials or electrokinetic effects (e.g., [16–20]). This effect is characterised by one coupling parameter, the streaming potential coefficient, defined as the ratio of the potential difference to the pressure difference. Electrokinetic effects have been observed in laboratory experiments with rocks (e.g., [21]); they lead to remarkable spatial and temporal variations of the spontaneous electric potential (SP) in natural conditions [22,17,23], especially near active volcanoes (e.g., [24]). The early observation on the tree trunk was confirmed by an experiment on a spruce tree [25], which in addition reported a non-linear relationship between the daily electric potential variation and the intensity of the solar radiation. Measurements at the surface of a chestnut tree [26] indicated that the time variations of the electric potential depend strongly on the season. In summer, clear daily variations of the trunk potential are observed, with a minimum in the afternoon when upper electrodes are referred to lower electrodes, in agreement with the previous experiments. In the late fall, after leaf shedding, these clear daily variations disappear, as expected if sap flow is the dominating mechanism for electric potential generation. However, electrical signals, with more erratic time variations, are still observed, indicating that other mechanisms may also contribute, possibly unrelated to sap flow. The electric potential was also monitored at several points of a Turkey oak (Quercus cerris) during 2 years [27,28]. This experiment indicated that the summer daily variations are in phase at the various points, with again a minimum of the potential with respect to the ground in the afternoon. The amplitude can vary by more than a factor of two from point to point. Two periods for large daily variations were observed: end of March and summer (end of June–July). Streaming potentials have also been studied in Salix alba L. sapwood samples in the laboratory and the results have been compared with the observed electrical daily variation in a standing tree to obtain estimates of the sap flow velocity [29]. The sap flow velocity, thus, estimated from the electrical variations, is 15–17 m h1, which is much higher than the accepted values for S. alba L., which are of the order of 2– 3 m h1[29]. The positive sign of the streaming potential coefficient obtained in the laboratory is in agreement with the sign reported for most rocks in usual natural conditions (e.g., [30]), but does not agree with the sign of the observed electric daily variation in the tree trunk. Indeed, for a positive streaming potential coefficient, the potential of the trunk should be positive with respect to the ground. While the observed daily variation could be reasonably interpreted at first in terms of streaming potentials, the relationship between the sap flow and
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the electric potential variation therefore remains puzzling. Other effects, such as thermo-electrical effects, membrane potential and experimental artifacts, need to be considered before a coherent physical interpretation can be proposed. It appears, therefore, interesting to undertake new experiments to investigate in more details the relationship between the sap flow and the electric potential variations in a tree. Monitoring of the electric potential in trees and more generally in living plants, may be interesting for other reasons. Electric activity has been evidenced in hibiscus and maize (e.g., [31,32]) and electrical signals have been observed in response to changes in transpiration and photosynthesis in willow plants [33] or Mimosa pudica [34]. The electric potential in trees may, therefore, reflect a combination of physical, chemical and physiological responses in relation with water transport, photosynthesis and adaptive feedback mechanisms. The seasonal variation of the electrical daily variation, for example, may be closely associated with the poorly understood seasonal variations of the enzymes of sucrose metabolism [35]. In this paper, we present a new experiment lasting more than 2 years in a poplar tree. In this experiment, we have focused on the spatial and temporal variations of the electric potential distribution in a single tree, using an increased number of electrodes compared with previous work. The comparison of several trees will be considered in a later stage. The experimental set-up is first presented. After a brief overview of the annual cycles of the tree, we present specific experiments performed to constrain the physical mechanisms. In particular, the electrical daily variations are compared with a direct and independent measurement of the sap flow with a thermal method. In addition, temperature effects, which can potentially affect the measured electric potential, are studied in details. In the conclusion, we discuss the generation mechanisms of electric potential in the tree trunk. 2. Experimental set-up 2.1. Electrode array The investigated tree is a poplar (Populus nigra L.) located in Remungol1 (Brittany, France). The first part of the experimental set-up, with a set of 26 electrodes, was installed on August 6, 2002, 21 electrodes in the trunk and five in two emerging roots (Figs. 1 and 2). Trunk electrodes are arranged in three groups: two circular rings and one vertical line. The lower ring, with eight electrodes numbered E1 to E8, is located 1.0 m above the ground and has a circumference of 2.7 m. The upper ring, with eight electrodes numbered E11 to E18, is located 3.4 m above the ground and has a circumference of 2.4 m. The vertical line comprises five electrodes numbered from E30 (0.5 m above the ground) to E34 (2.9 m above the ground) and aligned with E6 and E16 on the northern face of the trunk. Root electrodes E01, E02 and E03 (Figs. 1 and 2) are implanted in a root running 1 WGS 84 geographic coordinates: 47 560 0500 N and 2 530 4500 W, i.e. Universal Time used in figures is almost the same as the local Solar Time.
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Fig. 2. Plan view showing the canopy area, the trunk and the two roots equipped with electrodes. Also shown are the two Petiau electrodes, P1 and P2.
Fig. 1. General view (from west) of the array of electrodes shown as black dots on a simplified sketch of the tree. The box labelled T–H indicates the position of the outdoor temperature and humidity sensors.
eastward from the trunk, partially emerging from the ground. The diameter of this root is about 0.18 m, and the electrodes E01, E02 and E03 are at distances of 0.45, 0.90 and 1.35 m from the eastern edge of the trunk, respectively. Electrodes E04 and E05 are located at 0.6 and 1.2 m from the north-eastern basis of the trunk on a shallow root with a diameter of 0.15 m (Fig. 2). Seven electrodes (E21 installed on May 31, 2003, and E22 to E27 installed on August 18 and 27, 2004) were added along a vertical segment whose lower (E21) and upper (E26 and E27) ends are at 5.6 and 10.5 m above the ground, respectively (Fig. 1).
The electrodes have a diameter of 6 mm and were cut in stainless steel rods which were carefully degreased 1 day before the installation. The apparent metallic part of the electrodes is cut to 15 mm, and each electrode is connected by wrapping a cable which is secured with a epoxied cap of thermo-sheath (Fig. 3). The connectivity of an electrode with its cable is tested with an ohm-meter. The electrodes are inserted in the tree by drilling a hole with a diameter of 8 mm through the bark and another one with a diameter of 6 mm and a depth of 15 mm in the wood. Next, the electrodes are gently hammered until being embedded in the wood. In this way, the non-isolated metallic part of the electrodes is fully stuck in the wood so that the meteorological influences, such as rain or fast temperature changes are reduced. The contact resistance of the electrodes has been measured with an AC ohm-meter and varies from 4700 to 6400 V with an average of 5400 V. The electrode array is complemented with a nonpolarisable lead–lead chloride electrode [36] which is used as a reference for all potential measurements. This electrode is located 5.0 m away from the tree in the eastward direction (Figs. 1 and 2) and is buried at a depth of 0.7 m with clay as contact material. On May 31, 2003, another nonpolarisable electrode labelled E102, was buried using the same method at a depth of about 0.3 m near the root electrode E01. 2.2. Data acquisition system Data acquired at the beginning of the experiment are not used in the present study, and only those obtained with the digital acquisition system installed in November 2003 are presented here. The measurement device is a Keithley 2701 digital multimeter with an input impedance larger than 100 M V and equipped with a relay matrix having 40 measurement
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Fig. 3. Top: detailed view of an electrode. The apparent metallic part of the electrode is fully embedded in the wood. The epoxied cap secures the cable which is wrapped around the stainless steel rod. Bottom left: view of an electrode placed on the tree. The uncovered part of the electrode is fully embedded in the wood under the bark in order to reduce meteorological influences. Bottom right: in the Granier’s method, the sap flux is obtained by measuring the thermal flux advected by the sap flow with one heater (H) and two thermo-couples (T).
channels controlled through an acquisition software. Measurements of the electric potential are made at all electrodes with a sampling interval of 1 min. We use a UT time base, synchronised in real time to the Frankfurt atomic clock. Both the computer and the multimeter are powered with a backup generator which prevents breaks caused by short failures of the electrical power line. In order to check the entire electrical system, and in particular, the high input impedance of the recorder, we performed several injections of electrical current in the soil near the basis of the tree. The applied voltage at the grounded electrodes was 12 V for an electrical current of 2.5 mA. Fig. 4 shows the electrical potential measured at several
electrodes during two current injections of opposite signs. The response due to the injections is clearly seen on all channels. In addition, the electric potential response happens within one sampling time. This indicates that our measurements are not affected by artificial delay times or capacitive effects, that could, for example, have resulted from an insufficient input impedance of the acquisition system. Such tests are performed regularly. 2.3. Meteorological measurements In November 2003, a meteorological station was installed to record the main atmospheric parameters in the neighbourhood of the tree. The measured parameters include the speed and direction of the wind, the atmospheric pressure, the outside temperature and humidity, the rain events. Temperature and humidity are also measured indoor in order to identify a possible sensitivity of the electronic devices to the environmental conditions. All meteorological parameters are recorded every 15 min and synchronised with the time base used for the potential measurements. 2.4. Influence of temperature on the electrode array
Fig. 4. Electrical potential measured at several electrodes during an injection of electrical current in the soil near the tree. Hours are given in Universal Time.
Stainless-steel electrodes might be affected by significant temperature effects, and it is important to discuss purely thermal effects as the cause of the observed diurnal variations of the electric potential. In principle, this is possible, as the temperature sensitivity of the electrode–wood contact may be a
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present in the curve of the outdoor temperature measured in the vicinity of the tree (Fig. 1). This condition is, however, not due to a temperature effect at the electrodes, but to a global effect affecting the whole tree. This was further checked by studying the correlation between the potential and temperature curves. In particular, we observed that the correlation between the E6 and E31 potential curves is maximal for zero-time delay both before and, significantly, after the installation of the insulating pot on E31. Conversely, when the pot is installed, the correlation between the outdoor and E31 temperature curves is maximum for a time-delay of 45 min. This is another manner to demonstrate that the delayed correlation between electric potential and outdoor temperature results from the activity of the tree. 2.5. Sap flow measurements
Fig. 5. Thermal tests made on electrode E31 to verify that no important potential variations are induced by temperature. Potential at nearby E6 electrode and outdoor temperature are given for reference. The transient variations of E31’s potential are observed when introducing the warm (or cold) bottle in the box covering the electrode. Hours are given in Universal Time.
rapidly varying function of the water content in the wood and the air humidity. Temperature influence on the tree electrodes would introduce temporal effects depending on position. For instance, the amplitude of the potential variations should be larger on the south side exposed to solar heating. Note that this is not what we observe actually; however, dedicated thermal experiments were performed to check for a possible temperature effect on our electrode array. As shown by Petiau [36], the temperature sensitivity of the grounded electrochemical electrode used as as reference is negligible (smaller than 30 mV= C), and our thermal experiment focused on the steel electrodes. In August 2004, we applied large artificial thermal perturbations to E31 which was previously covered with an insulating pot. Fig. 5 shows the results obtained during both a heating and a cooling test done by introducing a bottle of hot water or ice in the pot. Excepted for sharp transient variations of the potential occurring when introducing the bottle, no perturbation of the E31 potential is observed when compared with the potential measured on the nearby E6 electrode. This clearly rules out a direct effect of temperature on the measured electrode potential. Looking at Fig. 5 more closely, we observe that potential variations at both E31 and E6 have features similar to those
During a limited period of time (from June 21 to July 15 of 2004), direct measurements were performed in addition to the electrode measurements. The sap flow is measured with the heat-balance technique initially proposed by Granier [9]. This method uses a pair of probes, each equipped with a small resistor to produce heat and a miniature thermocouple to measure the temperature inside the wood. The diameter of a probe equals 2 mm for a length of 20 mm. Only the upper heater is turned on and both probes are used to make differential temperature measurements in order to measure the thermal imbalance due to sap flow (Fig. 3). One pair of probes was placed in the root near E01 and two pairs were placed 10 cm apart between E31 and E32 (Fig. 1). The part of the trunk holding the probes was covered with an insulating blanket in order to attenuate the thermal perturbations produced by the atmospheric variable conditions. The temperature was measured every 5 min and these data were later converted into sap flow current through an experimentally derived calibration [9]. 3. Presentation of data 3.1. Overview of electric potential variations Figs. 6–9 present the data for seven electrodes from December 1, 2003 to May 21, 2005. This choice of seven electrodes is representative of the whole electrode array: one root electrode (E01), E6 on the lower ring, E11 and E18 on the upper ring, E34 located on the vertical line just beneath the upper ring, E21 and, when available, E25 located on the vertical line 5.50 and 9.50 m above the floor, respectively. Two breakdowns of long duration interrupt the curves, the first from January 12, 2004 to February 17, 2004, the second from September 4, 2004 to September 15, 2004. These recordings of long duration show that the electrical activity is present on all electrodes over the whole time span although with varying amplitudes and a high variability from one electrode to another. Large daily variations are present on most electrodes from spring to summer. A first important observation is the persistence of the electrical activity during
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Fig. 6. Top: potential signals measured on six electrodes representative of the entire electrode array for the December 2003–April 2004 period. Relative potential values. Bottom: outdoor temperature measured near the tree (see Fig. 1 for location). Tick marks fall at midday.
Fig. 7. Same as Fig. 6 for the April–August 2004 period.
Fig. 8. Same as Fig. 6 for the September 2004–January 2005 period.
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Fig. 9. Same as Fig. 6 for the January–May 2005 period.
winter (Figs. 6 and 8) when the tree activity is expected to be greatly reduced. During this period, a daily variation is observed on all electrodes, sometimes with a high amplitude as large as the one seen in spring and summer. This is, for example, the case for electrode E18 whose diurnal amplitude remains of the order of 30–50 mV all year long. Note that in December, the E6 curve appears to be the upper envelope of the E18 signal. In winter, the signals appear one-sided with daily positive jumps with respect to a smoothly varying base level. In spring and summer, this one-sided structure is less visible and replaced by a more symmetrical pattern. This is particularly clear when comparing the E18 curve in September and December 2004 in Fig. 8. At many points in the tree, long-term and daily electric potential variations appear anti-correlated with the variations of the outdoor temperature. This is, for example, the case for the long-term trends of E01 and E6 in December 2003 (Fig. 6), or for the long-term trend and the daily variations of E6 March– April 2004. Note, however, that in March–April 2004, there is no clear relationship between E01 and the temperature,
indicating that this anti-correlation between electric potential and temperature is complex and time-dependent. When considering the diurnal signal of a given electrode on a long-term basis (Figs. 6–9), larger temperature daily variations are not systematically associated with larger electrical diurnal amplitudes as would be expected for a dominant temperature effect. These observations, together with the thermal tests discussed above, rule out the hypothesis that the observed electrical variations are due to a purely thermal artifact at the electrical contact between steel and wood. Instead, a physical mechanism indirectly connected to the temperature and involving the activity of the tree must be invoked, as proposed by previous authors. Additional peculiar observations are made when looking at the period from February to March 2004, a period which is also shown with an enlarged time scale in Fig. 10. During this period, all electrodes, except electrode E18, display large negative peaks, for example, around February 23, March 7 or March 13 (Fig. 10), while E18 shows a more regular daily variation. Interestingly, these large negative peaks on the
Fig. 10. Enlargement of a part of Fig. 9 showing the occurrence of negative daily jumps of the electric potential (E6, E34, E11 and E21) corresponding to negative outdoor temperature. Notice the persistence of the daily positive jumps for electrode E18. Tick marks of horizontal axis fall at midday.
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Fig. 11. (a) Sap flow measured with two probes located near E32. (b) Outdoor temperature. (c) Electrical potential measured at E32. (d) First time-derivative of the E32 potential shown in (c). Tick marks of horizontal axis fall at midday.
potential occur precisely when the temperature goes below zero. The same phenomenon is observed during the winter of 2004–2005 (Fig. 9), especially in the second half of February 2005. The zoomed signals shown in Fig. 10, reveal the occurrence of dipolar transient signal with a duration of several hours on March 3 and 6, 2004. Such signals frequently occur with a duration varying from several minutes to several hours. The amplitude of the dipolar signal increases with the altitude of the considered electrode, a feature observed for all similar signals we examined, which rules out the possibility that these signals are caused by instabilities of the reference ground electrode. The amplitude of these transient signals depends more strongly on altitude than observed for the step-like signals recorded during the test of current injection in the soil (Fig. 4). It is then unlikely to explain these transient signals by invoking telluric currents, either natural or anthropic, originating from the ground. Rain or storms, which could have been a first explanation, must also be excluded using our meteorological data. The origin of such signals, which appear occasionally, remains unclear and deserve further study. A big change occurs in the recorded signal from winter to spring in both years 2004 and 2005 with the onset of a stable daily activity at all electrodes. This onset is particularly clear in April and May of years 2004 (Fig. 7) and 2005 (Fig. 9) with starting times differing of several weeks from one electrode to another. For instance, activity begins around March 20, 2005 for E18 and around May 1, for E25 (Fig. 9). Once established, the daily activity remains high during summer and autumn, and the return to the low winter activity also occurs at noticeably different dates depending on the electrode (Fig. 8). 3.2. Comparison with sap flow measurements We now turn to the comparison between electrical signals and sap flow measurements. The sap flow curves corresponding
to the probes located near E32 are shown in Fig. 11 a for the period going from June 21 to July 15, 2004. The two curves show clear diurnal variations; they have a similar appearance but their amplitudes differ up to a factor of two on certain days. The electrical potential (Fig. 11c) measured at E32 and its first time-derivative (Fig. 11d) also show a diurnal variation with a variable amplitude which does not appear to be directly related to the amplitude of the sap flow. The same temporal variation of the electrical signal was observed during the days preceding the installation of both the thermal probes and the insulating blanket. This ensures that the electrical variations are not due to the heating device. To look more closely at the correlation between the electrical signal and the sap flow, a period of 4 days was selected (Fig. 12). This detailed view allows to examine precisely the temporal coincidence between the sap flow and the electrical variations, either in the potential curve or in its time-derivative. The variations goes from the early time in the morning, when the sap flow begins to be reactivated, to the mid-morning when the sap flow reaches its maximum value. During this period of sap flow reactivation, the timederivative of the potential curve shows a conspicuous bipolar variation with a high amplitude, beginning with a positive lobe. The late negative lobe of the bipolar event reaches its minimum value (black dashed line) precisely when the sap flow stops increasing and reaches a plateau. At that time, the potential begins to decrease and becomes minimal slightly after the sap flow has left its plateau-level and begins to diminish sharply. The electrical potential then returns to its original value in about 8 h, while a zero sap flow is reached faster, after about 4 h. The time when zero sap flow is reached (red dashed line) or keeps decreasing slowly asymptotically to zero, also coincides approximately with the maximum of the time-derivative of the electrical potential. Notice that a large electrical signal still remains while the sap flow has completely vanished.
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Fig. 12. Same as in Fig. 11 for a limited period showing the correlations between electrical and sap flow events. Hours are given in Universal Time.
electrodes. Our new observations make this interpretation quite questionable. Indeed:
4. Discussion In the rather small number of experiments made on standing trees, listed in the introduction, the measured electric potentials were attributed to an electrokinetic effect forced by the sap flow [15,26,25]. The rough agreement of the value of the electrokinetic coupling coefficient measured in the laboratory with the value required to account for the observed magnitude of the potentials in the standing tree was taken as a strong clue in favour of this hypothesis, although the sign does not appear to be the correct one. Furthermore, these previous experiments were generally performed over short time periods, with few
(1) A negative potential is observed on all the trunk electrodes with respect to the ground. (2) In the framework of electrokinetic theory, the electric field is proportional to the pressure gradient, hence, to the sap flow per unit surface. This implies, at least in average, for example, taken over the eight electrodes of a ring, a linear increase of the electric potential amplitude with height in the trunk (recall that the reference electrode is located in the ground). This variation is not observed at all (Fig. 13).
Fig. 13. Amplitude of the electric potential variation from the 5:00 a.m. to 5:00 p.m. period of June 1, 2004.
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(3) The heterogeneity of the diurnal amplitudes of the electric potential from electrode to electrode is difficult to explain in terms of an electrokinetic effect. Of course, we may expect lateral heterogeneity in the xylem vessels through which the sap is pumped up. However, the tree is a conducting medium, and some homogenisation of the potential at a given height is expected. (4) The strongest argument comes from the comparison of the electric potential curves with the sap flow curves (Figs. 11 and 12). Clearly, the electric potential is not at pace with the sap flux, assuming that the thermal method measures the sap flux with negligible retardation. Actually, our measurements of the sap flow at two different points provide the same time variation and support this assumption. In particular, we note that a strong negative potential is still present after the sap flow has receded, around 10 p.m. (Fig. 12); it is at this very moment that the curve of the time-derivative of the potential reaches its maximum value. Similarly, in the morning, during the 2-h time interval taken by the sap flux to reach its maximum, the electric potential hardly changes. These observations cannot be reconciled with the electrokinetic mechanism in its simple form. (5) The electric potentials in a root and in the nearby soil are not equal (Fig. 14), suggesting the presence of an electrical barrier between the tree root system and the soil. Nevertheless, the curves of Figs. 11 and 12 evidence a stable functional relationship between the sap flow and the electric potential. To simplify the picture, it appears that the sap flow polarises (electrifies) negatively the whole tree trunk with respect to the ground; but this polarisation process has a long time constant, on the order of hours; when the sap flow vanishes, in the evening, it is with this long time constant that the polarisation also goes to zero. Another remarkable fact is that the rapid onset of the sap flux in the morning generates a specific transient variation on the electric potential, particularly outstanding in its time-derivative (Fig. 12).
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A well known phenomenon in geophysical prospecting, although still poorly understood, is the so-called induced polarisation (e.g., [37,38]). Injecting electric current into the ground through two electrodes generates an electric field in their neighbourhood; when switching off the current source, the potential goes back to zero with a time constant which can sometimes reach several seconds, depending on the nature of the ground and of the electrodes (e.g., [39,37]). Such induced polarisation effects can be particularly strong in the presence of ore deposits, which is the basis of its use as an empirical prospecting method. This observation reveals the ubiquitous presence of electromotive forces in the ground after turning off the external current source. In their absence, the ground would be back instantaneously equipotential. However, the time constant involved in the present experiment is so large that it seems necessary to call for a mechanism specific to biological living systems. Note that all the curves corresponding to the different electrodes behave in a similar fashion with respect to the sap flow curve, while the amplitudes of this daily variation differ greatly from point to point. This time constant does not appear specific to a given neighbourhood but characterises the whole tree. The mechanism that could be invoked to generate such a trunk polarisation and time constant remains unclear. As mentioned in the introduction, the observed electric potential may reflect a combination of physical, chemical and physiological responses to the sap flow, photosynthesis and adaptive feedback controls of the tree. While we are not able to propose a comprehensive model at this stage, we can sketch the following scenario. We have to find a mechanism able to accommodate the peculiar electrical system observed in the tree trunk. The trunk is a conductor, but the electrical potential, which depends on the position vector r and time t, must be able to sustain a temporal relaxation of the form: @Vðr; tÞ Vðr; tÞ þ ¼ F½r; SðtÞ; @t t
(1)
Fig. 14. Example of diurnal potential variation measured on a chemical electrode (E102) placed in the soil near the root electrode E01. Note the different vertical scales used for both potential curves (left scale for E01 and right scale for E102). Major tick marks of horizontal axis fall at midday.
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Fig. 15. (a) Main electrical structure of a sectional cross-section of the tree trunk. Small longitudinal capacitive elements are composed by insulating xylem elements embedded in the conductive trunk and containing the circulating and conducting sap (b).
where t is some relaxation time and F is some positiondependent functional of the sap flow SðtÞ, vanishing when the sap flow vanishes. As t is of the order of several hours, some poorly conducting medium must be present within the conductor, able to generate a significant capacitance. In addition, we know that F is a negative function of S, basically constant with height z, but smoothly varying around the circumference. This imposes a configuration of the source with translational symmetry along the tree axis, as depicted in Fig. 15 a. The spatial configuration of the potential results from leakage of charge accumulated within this supposed nonperfect isolator. Note that a grounded perfect conductor with an inner distribution of charge is characterised by constant potential and spatially varying surface charge distribution. Here, we have a non-perfect insulator embedded in a non-perfect conductor, which allows to maintain a small volume current. As the potential varies with azimuth, we have to conclude that the charge distribution maintained by the insulator is not
cylindrical. This probably requires a non-cylindrical sap flow as well. In our tree, given the asymmetric distribution of branches and roots around the axis of the trunk (Fig. 2), it may not be unexpected. Note that the two measurements of sap flow also support a non-cylindrical sap velocity. At each electrode, the potential is the result of the potential distribution due to sum of all the individual electrical sources, namely the leakage of all the supposed elementary capacitors (Fig. 15). Once this electrical mechanism is proposed, the role of the sap flow can be sketched as follows. Let us consider a xylem element (Fig. 15b). The conducting sap pervades the trunk and makes it a conductor; when photosynthesis and transpiration are active, it is circulating upwards in xylem elements. The walls of such elements are made of insulating ligneous cell walls. In the case of a solid rock surface, elementary charges are adsorbed, creating an excess charge in the electrolyte. It is the motion of this excess charge that creates the electrokinetic effect. In our case, however, a different situation happens, which completely changes the resulting distribution of currents. Indeed, imagine that the electric charges are not just adsorbed at the solid surface, but are now allowed to freely diffuse within the wall. What now dominates the electrical current is not the circulation along the axis of the trunk but the radial charge transfer. When the sap flow is suppressed, the charge carriers slowly diffuse back to the sap electrolyte or alternatively may get neutralised within the wall. This situation is analogous to a heat source in an underground cavity [40]. The temperature in the cavity during heating is rising linearly after some time, corresponding to a steady state heat transfer from the cavity to the surrounding rock. When the heat source is removed, the temperature is going back to the initial state, but with a dynamics controlled by the diffusion of heat in the walls. If this analogy is relevant for the tree potential, then the relaxation should actually not be exponential but a power law of time. The data in the tree at this time do not allow to distinguish between the two different types of relaxation. To summarise, we propose that the spatio-temporal characteristics of electrical potential in the tree trunk might be explained by a biological mechanism allowing the diffusion of charge carriers (e.g., heavy protein fragments or charge carrying hormones) across the insulating gel of the xylem walls. Maybe this charge transport is controlled actively by dedicated ionic channels in the wall, followed by molecular diffusion once across the membrane. Such a mechanism then suggests the presence of electrically active structures within the xylem channels. Thus, the xylem may play a more active role in the electrical response than would have been expected from nonliving cells with pure conduction. 5. Conclusion This experiment confirms the existence and largely extends the investigation of specific daily variations of the electric potential distribution in a tree trunk as mentioned in previous studies [15,26–28]. These daily variations bear a definite relation to the simultaneously sap flow in summer. The
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observations of electrical variations in winter would then imply a sporadically varying sap flow, both in space and time, during this season. These results, deduced from measurements on a single tree, should be confirmed by performing analogous studies on several trees in order to get a statistical significance. While the order of magnitude of the observed variation is the same as observed by previous workers, an electrokinetic mechanism seems to be unable to account for the independence of the potential with respect to altitude. Instead, we propose a different mechanism based on charge diffusion from the conductive sap flow channels into the resistive xylem walls. This mechanism could be clarified by a dedicated experimental program, for instance, by performing measurements on small trees in the laboratory or by using ion-selective microelectrodes or energy dispersive X-ray microanalysis. Thus, electrical monitoring of a living tree can reveal both unexpected patterns of the sap flow and new mechanisms of charge exchange in xylem elements. These results should raise a renewed interest in electrical measurements in trees. Experiments with long-term monitoring using a large number of distributed electrodes are needed to make progress. Acknowledgments The authors thank Fre´de´ric Conil for technical assistance and Pierre Morat for guidance. This work is IPGP contribution no. 2149. We thank M.L. Gicquel for providing us with facilities during the experiment. This work was financially supported by the CNRS and ANDRA through the GdR FORPRO and corresponds to the GdR FORPRO contribution number 2006/03 A. References [1] S. Lebaude, N. Le Goff, J.-M. Ottorini, A. Granier, Carbon balance and tree growth in a Fagus sylvatica stand, Ann. For. Sci. 57 (2000) 49–61. [2] L. Lambs, M. Berthelot, Monitoring of water from the underground of the tree: first results with a new sap extractor on a riparian woodland, Plant Soil 241 (2002) 197–207. [3] L. Lambs, J.-P. Loudes, M. Berthelot, The use of the stable oxygen isotope (18O) to trace the distribution and uptake of water in riparian woodlands, Nukleonika 47 (2002) 115–155. [4] J.D. Johnson, R. Tognetti, P. Paris, Water relations and gas exchange in poplar and willow under water stress and elevated atmospheric CO2, Physiol. Plant. 115 (2002) 93–100. [5] L. Meiresonne, N. Nadezhdin, J. Cermak, J. Van Slycken, R. Ceulemans, Agric. Forest Meteorol. 96 (1999) 165–179. [6] A. Granier, P. Biron, D. Lemoine, Water balance, transpiration and canopy conductance in two beech stands, Agric. Forest Meteorol. 100 (2000) 291– 308. [7] L. Lambs, E. Muller, Sap flow and water transfer in the Garonne river riparian woodland, France: first results on poplar and willow, Ann. For. Sci. 59 (2002) 301–315. [8] R.H. Swanson, Significant historical developments in thermal methods for measuring sap flow in trees, Agric. Forest Meteorol. 72 (1994) 113–132. [9] A. Granier, Mesure du flux de se`ve brute dans le tronc du Douglas par une nouvelle me´thode thermique, Ann. Sci. For. 44 (1987) 1–14. [10] A. Guevara-Escobar, W.R.N. Edwards, R.H. Morton, P.D. Kemp, A.D. Mackay, Tree water use and rainfall partitioning in a mature poplarpasture system, Tree Physiol. 20 (2000) 97–106. [11] R. Benyon, Nighttime water use in an irrigated, Eucalyptus grandis plantation, Tree Physiol. 19 (1999) 853–859.
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