Tree Physiology 26, 1277–1288
© 2006 Heron Publishing—Victoria, Canada
Vertical and horizontal water redistribution in Norway spruce (Picea
abies) roots in the Moravian Upland
NADEZHDA NADEZHDINA,1,2 JAN ÈERMÁK,1 JAN GAŠPÁREK,1 VALERIY NADEZHDIN1
and ALOIS PRAX1
1
Institute of Forest Ecology, Mendel University of Agriculture and Forestry, Zemedelska 3, 61300 Brno, Czech Republic
2
Corresponding author ([email protected])
Received July 8, 2005; accepted December 6, 2005; published online June 30, 2006
Summary Hydraulic redistribution (HR) by roots of large
Norway spruce (Picea abies (L.) Karst.) trees was investigated
by means of sap flow measurements made with the heat field
deformation method. Irrigation was applied to a limited portion of the root system to steepen gradients of water potential in
the soil and thus enhance rates of HR. On completion of the sap
flow measurements, and to aid in their interpretation, the structure of the root system of seven of the investigated trees was exposed to a depth of 30 cm with a supersonic air-stream (airspade). Before irrigation, vertical redistribution of water was
observed in large coarse roots and some adjacent small lateral
roots. Immediately after localized irrigation, horizontal redistribution of water from watered roots to dry roots via the stem
base was demonstrated. The amount of horizontal distribution
depended on the position of the receiving roots relative to the
watered roots and the absorbing area of the watered root. No redistribution from watered roots via dry soil to roots of neighboring trees was detected. Responses of sap flow to localized
irrigation were more pronounced in small lateral roots than in
large branching roots where release and uptake of water are integrated. Sap flow measurements with multi-point sensors
along radii in large lateral roots demonstrated water extraction
from different soil horizons. We conclude that synchronous
measurements of sap flow in both small and large lateral roots
are needed to study water absorption and transport in tree root
systems.
Keywords: heat field deformation method, lateral roots, localized irrigation, multi-point sensors, sap flow, single-point sensors, supersonic air-spade.
Introduction
The importance of hydraulic redistribution (HR)—the passive
movement of water from wet to dry soil via roots—has been
well documented in woody plants over the last two decades
(Richards and Caldwell 1987, Caldwell and Richards 1989,
Dawson 1993, Burgess et al. 1998, Smith et al. 1999, Scholz et
al. 2002). Water can be hydraulically redistributed upward
(Caldwell et al. 1998, Horton and Hart 1998), downward
(Schulze et al. 1998, Smith et al. 1999) or horizontally (Brooks
et al. 2002, Sternberg et al. 2002, 2004, Smart et al. 2005). To
date, most investigations of HR have been carried out in regions with a pronounced dry season under semi-arid (Burgess
et al. 1998, Hultine et al. 2003), Mediterranean (Burgess et al.
1998, 2000b, Nadezhdina et al. 2004b) or Brazilian savanna
(Cerrado-type) (Scholz et al. 2002, Moreira et al. 2003) conditions. However, even short-term drought (lasting several
weeks) in wetter environments may present serious constraints
on plant functioning and survival and HR may play an important role during these times. Furthermore, HR during drought
may be particularly important for trees having shallow root
systems, such as Norway spruce (Picea abies (L.) Karst.).
Previous studies suggest that plant root systems can rapidly
change their spatial pattern of water uptake in response to the
application of water (Èermák et al. 1993, Cabibel 1994, Green
and Clothier 1995, Clothier and Green 1997, Fernandez et al.
2001). However, the mechanism by which locally applied water is transferred via roots to dry soil has not been identified. In
a study of the effects of localized application of deuterated water in two contrasting Pacific Northwest forest types, measurements of soil volumetric water content at multiple depths and
of sap flow in roots revealed horizontal redistribution of water
via superficial lateral roots (Brooks et al. 2002). The results
indicated that resistance of the transport pathway for water
was lower between roots on the same side of the tree than between roots on opposite sides of the tree.
Sap flow measurement seems to be one of the best ways of
studying HR, but methods allowing bidirectional sap flow
measurements (acropetal and basipetal) are necessary. Such
methods include the heat ratio method (HRM; Marshall 1958,
Burgess et al. 1998, 2000a, 2001a), the heat field deformation
method (HFD; Nadezhdina et al. 1998, 2004a) and the modified heat dissipation technique (Brooks et al. 2002). The second fundamental requirement of a sap flow method suitable
for studying water redistribution by roots is high sensitivity at
low flow rates because the reverse night flows of hydraulically
redistributed water are usually low. Methods allowing flow
rates at different sapwood depths to be distinguished are informative for studying links between root structure and function-
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NADEZHDINA ET AL.
ing. Measurements of the radial pattern of sap flow in roots or
stem bases combined with experimental manipulations (e.g.,
local watering) can provide insight into the changing patterns
of root functioning during drought (Nadezhdina and Èermák
2003).
In this study, localized irrigation was applied to dry topsoil
to increase the rate of horizontal HR. Water was applied to a
small area between several Norway spruce trees growing at
various distances from the point of irrigation. Building on
findings by Brooks et al. (2002), we examined roots on the side
of each tree facing the irrigated area. We determined: (1) the
direct transport pathways of water by measuring sap flow in
small and large roots close to the stem base where information
about the flow rate and direction is integrated; and (2) the rates
of sap flow response to a sudden change in the driving forces in
roots of different sizes and at different distances from the point
of irrigation.
Material and methods
Site, sample trees and meteorological conditions
The experimental site was at the Mendel University Training
Forest Enterprise “Krtiny,” Stand 20C3b “Krmelec”, located
in the Vranov forest district, in southern Moravia, Czech Republic (49°18,410′ N, longitude 16°35,864′ E, altitude 460 m
a.s.l.). A small flat experimental plot of pure Norway spruce
was chosen for study. Stocking density of the experimental
plot was 1365 stems ha –1, basal area was 29.95 m 2 ha – 1, mean
height was 20 m, projected crown area was 8339 m 2 ha – 1 and
LAI was 11.6. The age of the trees was 26 years. The site had
been an old field that had since become afforested, and regular
furrows in the east–west direction were still visible. Seven
neighboring sample trees were selected (Table 1). There were
four sample trees (Trees 1–4) in one row and three trees
(Trees 5–7) in a second row (Figure 1).
At the site, mean annual precipitation is 620 mm and mean
annual temperature is 7.5 °C. The experiment was carried out
from June 8–10, 2003, when the weather was unusually warm
and dry for the time of year. The main meteorological parameters (air temperature and humidity, and global radiation) were
measured at a meteorological station situated 2 km from the
experimental plot. The station was equipped with a Model
EMS 33 microprocessor-controlled air temperature and humidity sensor, a Model EMS 11 global radiation sensor and a
Minikin TH & RT datalogger (EMS, Brno, Czech Repulic).
Localized irrigation
Irrigation was applied at a point between Trees 2, 3, 4, 5 and 6
(Figure 1). Based on the orientation of parts of the large lateral
roots visible at the ground surface, we assumed that one pair of
monitored roots of Trees 4, 5 and 6 was within the irrigated
area, and one pair of roots of each tree was outside the irrigated
area. There was a depression in the soil surface at the point of
irrigation, which ensured that there was no irrigation runoff.
Trees 1 and 7 were far from the point of irrigation (Figure 1)
and thus, none of the roots of these trees received water di-
rectly. To determine the pretreatment behavior of roots during
drought, no irrigation was applied during Day 1 of the experiment. On Day 2, we applied 115 l of water during late afternoon (after 1700 h). An additional 175 l was added at the same
location on the following morning at about 1000 h. The
amount of water applied was around 70 mm, which was close
to the monthly precipitation during summer.
Soil measurements
The soil was a loess-sandy to sandy-modal cambisoil on
weathered granodiorite, with an admixture of gravel (Prax and
Pokorny 2005). Volumetric soil-water content was measured
gravimetrically. Soil was sampled with a Kopecky ring, comprising a stainless steel open-ended cylinder (6 cm in diameter,
3.55 cm deep, with a volume of 100 cm 3 ), which was driven
into the soil with a hammer in three soil pits on Day 4 of the experiment (the day after the second irrigation was applied). Pit 1
was outside the experimental plot and served as a control (Figure 1). The other pits were in the middle of the plot: Pit 2 (irrigated) was at the edge of the irrigated area and Pit 3 (non-irrigated) was within 2 m of the irrigated area and within the zone
of the non-irrigated pairs of the sample roots of Trees 4 and 5.
Soil samples in the each pit were taken from four depths (4–9,
12–17, 20–25 and 30–35 cm).
Sap flow measurements
Method for sap flow measurements Sap flow in all sampled
roots was measured by the heat field deformation (HFD)
method (Nadezhdina et al. 1998, Nadezhdina and Èermák
2000a, Èermák et al. 2004), which is based on the measurement of changes in the heat field around a linear heater caused
by water movement. Deformation of the heat field was determined as a function of the ratio of two temperature differences,
recorded in the axial and tangential directions from the heater
by two pairs of differential thermocouples (Figure 2). The
thermocouples of the symmetrical pair, which measured the
symmetrical temperature differences (dTsym ), were placed
equidistant, Z ax (1.5 cm), from the heater in an axial direction
along the root. The thermocouples of the asymmetrical pair
measured the asymmetrical temperature difference (dTas ). The
upper thermocouple of this pair was situated in a tangential direction from the heater at distance Z tg (0.5 cm). The lower ends
of both differential thermocouples were inserted in the same needle. This arrangement of thermocouples around a heater allows
measurements of bi-directional (acropetal and basipetal) and very
low sap flow rates (Nadezhdina 1998, 1999, Nadezhdina et al.
2004a). Because accurate spacing of the thermocouples and
needles is a precondition for precise estimation of absolute
zero flow and changing sap flow direction, a template was used
during the installation of the single-point sensors. A special
tool was used to install the long needles of the multi-point sensors to keep them in parallel.
Sap flow calculation Sap flow (q; cm 3 cm – 1 h – 1 ) for a certain
root section i was calculated as:
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Table 1. The main biometrical parameters of the sample Norway spruce trees and the positions of the sap flow sensors in large and small lateral
roots. Abbreviations: DBH = diameter of breast height; and WRAA = watered roots absorbing area.
Sample tree
DBH
(cm)
Width × height of roots
(cm)
Sensor number, size
of root and root pairs1
Position of root relative to irrigation
and amount of WRAA2
1
14.6
5.7 × 5.7
2.4 × 2.4
10.2 × 14
2.3 × 2.3
2.3 × 2.3
3.3 × 3.3
8.0 × 12.5
3.5 × 3.5
7.7 × 13
3.8 × 3.8
8.8 × 11
3.6 × 3.6
8.3 × 12
3.3 × 3.3
8.5 × 15
4.0 × 4.0
4.5 × 5.5
2.7 × 2.7
5.3 × 10.5
4.7 × 4.7
6.0 × 11
4.5 × 4.5
1W
1w
2W
2w
2sw
3w
4N
4n
4NW
4nw
5SE
5se
5NE
5ne
6SE
6se
6NE
6ne
7SE
7se
7NE
7ne
0
2
3
4
5
6
7
1
2
22.6
10.0
17.8
28.1
24.5
22.2
–
*
**
*
***
*
–
–
–
–
–
***
–
**
**
–
–
0
0
0
0
Sensor number includes the sample tree number and the root orientation relative to the stem base. Small letters denote single-point sensors on
small roots and capital letters denote multi-point sensors on large roots. Root pairs are indicated by the same letters.
Symbols: 0 = non-irrigated tree; – = non-irrigated root; * = irrigated root with a small WRAA; ** = irrigated root with a medium-sized WRAA;
and *** = irrigated root with a large WRAA.
Figure 1. The root systems of
the experimental Norway
spruce plot, partially exposed
with an air-spade following the
sap flow measurements. For
details of the scheme of sensor
installation see Table 1. White
filled circles mark the positions of the single-point sensors and black filled circles
mark the positions of the
multi-point sensors. Small lateral roots measured by single-point sensors are shown in
white and large laterals measured by the multi-point sensors are shown in black. Black
dashed lines mark the area of
localized irrigation. Black
open circles indicate the positions of soil pits, where soil
water content was measured.
White open circles with numbers inside indicate the positions and numbers of the
sample trees.
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For small roots it was assumed that the entire xylem cross
section was uniformly conducting and sap flow was homogeneous along the xylem radius. Therefore, sap flow per small
root (Q) was calculated by multiplying sap flow density by
conducting xylem area.
Almost all large roots had highly asymmetric cross sections
and an uneven pattern of flow along the xylem radius. For this
reason, we did not scale these measures up to the whole-root
level, but studied only the qualitative variation in sap flow in
the different root xylem layers.
Figure 2. Schematic view of the heat field around a linear heater at
zero (thick ellipse), positive (left) and reverse (right) flow directions
(shown by thick arrows). Two temperature gradients, dTsym and dTas
(symmetrical and assymetrical, respectively), were measured by two
pairs of differential thermocouples (shown by open circles) and a third
temperature gradient (between the upper ends of both differential
thermocouples) was calculated as: dTsym – dTas . The value of dTsym
provides precise measurements of zero flow and flow direction. The
temperature gradients, dTas and (dTsym – dTas ), were used to calculate
positive and reverse flows, respectively.
q i = 3600 D
Z ax ⎛ K + dTsym – dTas ⎞
⎜
⎟
Z tg ⎝
dTas
⎠
(1)
where 3600 transforms seconds to hours; dTsym and dTas are the
temperature differences (K), recorded by the symmetrical and
the asymmetrical pair of thermocouples, respectively; Z ax is
axial distance between the upper end of the symmetrical thermocouple and the heater; Z tg is tangential distance between the
upper end of the asymmetrical thermocouple and the heater; K
is the value between both measured temperature gradients under conditions of zero flow (dTsym – dTas ) 0 and is determined
empirically from the relationship between the measured temperature differences and their ratio, dTsym /dTas ; and D is thermal diffusivity of fresh wood (cm 2 s –1 ). A nominal value for D
was given by Marshall (1958) as 2.5 × 10 – 3 cm 2 s –1. Based on
recent publications (Burgess et al. 2001a, Scholz et al. 2002),
where lower values were given, we assumed a nominal value
for D of 2.25 × 10 – 3 cm 2 s –1.
The same sensor configuration was used to measure reverse
flow, but flow direction (and therefore, a different calculation
of the sap flow from the measured temperature gradients) had
to be taken into consideration (Figure 2). When recorded diurnal values of dTsym become negative, Equation 1 automatically
transforms to:
q i = –3600 D
Z ax ⎛ – K + dTas ⎞
⎜
⎟
Z tg ⎝ dTsym – dTas ⎠
(2)
Sap flow sensors We used two types of sensors for sap flow
measurements: single-point sensors for small lateral roots and
multi-point sensors (where five thermocouples were inserted
in each sensor’s needle from 6 to 10 mm apart) for large lateral
roots where variability of sap flow along the root radius was
studied. The diameter of the small roots was about 3–5 cm and
the diameter of large roots varied from 6 to 13 cm. The heater
and the thermocouples of each sensor were placed in stainless
steel hypodermic needles (1 and 1.5 mm in diameter for the single- and the multi-point sensors, respectively). Each pair of
thermocouples was placed at the same depth below the cambium in the root xylem to measure temperature differences in
the common chosen “tangential section” of a root, perpendicular to the xylem radius. The temperature data were recorded at
1-min intervals with Unilog data loggers Midi-12 (EMS, Brno,
Czech Republic) and with DL2e loggers (Delta-T Device Ltd,
Cambridge, U.K.) using differential channels.
Sensor installation To examine variability in sap flow along
the radius of a large lateral root, a preliminary experiment was
carried out on the 5NE root of Tree 5. The multi-point sensor
with distances of 10 mm between measuring points was installed in the root at a distance of around 30 cm from the stem
base two days before the main experiment (Figure 3). After
1 day of monitoring sap flow, the position of this sensor was
moved about 40 cm upward and installed at the stem base in the
proximal zone of the same root where the sensor remained
during the main experiment.
For the main experiment, sap flow sensors were installed in
five sample trees (Trees 2 and 4–7): the single- and multipoint sensors were installed in two pairs of lateral roots (one
small and one large, respectively) close to the stem base
(30–80 cm from the stem base with the exception of sensor
5NE, which was left at the stem base). All the examined roots
were chosen from the side of the trees facing the site of local irrigation (Figure 1). Each pair of roots from the same tree was
differently oriented (Table 1). We measured the two smaller
sample trees (Trees 1 and 3) less intensively: we installed one
pair of multi-point sensors and one pair of single-point sensors
in the west-oriented roots of Tree 1 (diameter at breast height
(DBH) = 14.6 cm) and one single-point sensor in the small
root of the smallest tree, Tree 3 (DBH = 10 cm). Altogether
12 single-point and 10 multi-point sensors (with five measuring thermocouples each) were installed, allowing simultaneous measurements of sap flow at 62 points in the seven study
trees.
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where Q (cm 3 h – 1 ) is flow from roots, Ψdry (MPa) is the water
potential at the driest location (soil or needles), Ψ wet is the water potential of wet soil, R (MPa h cm – 3 ) is resistance of the
water pathways (depending on their length, and hydraulic conductivity), and A is relative root absorbing ability, which is a
function of the root’s absorbing area and takes into account a
relative increase in root absorption (expressed through the watered root absorbing area, WRAA) in response to localized
irrigation (relative units):
A=
( f (DRAA) + f ( WRAA))
f (DRAA)
(4)
where DRAA is the root’s absorbing area before irrigation.
Before the localized irrigation, A = 1. The magnitude of the increase inflow was expected to be higher for roots having
higher WRAA after irrigation. We did not investigate the relationship between flow rate and WRAA quantitatively, but
chose to focus on its functionality.
Results
Figure 3. The experiment in which the radial profile sensor was
moved along large Root 5NE. (A) Excavated root system of Tree 5
showing two sensor positions (1 and 2) on root 5NE. Note the large
number of sinker roots joined to Root 5NE between the two sensor positions. (B) Radial patterns of sap flow in Root 5NE at different sensor
locations. Filled squares denote radial patterns of sap flow measured
at the first sensor position during the day (dashed line), just before
moving the sensor and at night (1700 h; solid line). Open triangles denote radial patterns of sap flow measured at the second sensor position
during the day (dashed line) just after moving the sensor and at night
(1700 h; solid line).
Root excavation with a supersonic air stream
To explain sap flow behavior in different roots during the experiment and to link the function of a Norway spruce root system with its structure, the root systems of the sample trees
were partially exposed between the sample trees with a supersonic air-stream or air spade (Rizzo and Gross 2000, Nadezhdina and Èermák 2003) (air-spade model 150/90; AirSpade Technology, Verona, PA) (Figure 1). The nozzle was
connected to an Ingersoll-Rand compressor supplying 8–
10 m3 min –1 of air at a pressure of 1 MPa. Mean depth of the
excavated roots was about 30 cm, but in some places (where
sinker roots were found) we excavated to a depth of 80 cm.
Radial flow variation in the proximal zone of root 5NE
Large differences in radial patterns of sap flow were recorded
during the preliminary experiment when the same sensor was
placed at two positions 40 cm apart in the same 5NE large lateral root of Tree 5 (Figure 3). High flow rates were recorded in
all measured xylem layers during the night at the initial position of the sensor 30 cm from the trunk base. During the night,
the highest sap flow rate was recorded in the innermost xylem
layer measured (43 mm below the cambium) and the lowest
flow rate was observed in the two outer xylem layers (3 and
13 mm below the cambium). When the sensor was moved
40 cm up the root, all flow rates were substantially lower than
at the initial position. Nighttime sap flow rate remained relatively high at a depth of 43 mm below the cambium (Figure 3;
new sensor position); however, nighttime flow at the other
depths became negative (with the same magnitude for all measured layers). At the new sensor position, sap flow rate remained highest in the inner xylem during both the day and
night, with gradually decreasing rates toward the cambium.
This pattern contrasted with the daytime sap flow at the initial
sensor position where sap flow did not appear to differ across
xylem depths.
Environmental conditions during the main experiment
Modeling of horizontal water redistribution by roots
To explain responses of the sap flow of different roots to localized irrigation, a conceptual model of horizontal water redistribution was applied. The magnitude and direction of flow,
transferred horizontally via roots from the wet to the dry soil or
to the crown, was described by a simple equation that assumed
no xylem capacitance:
Q = ( f ) A( Ψ dry – Ψ wet )R – 1
(3)
Winter and spring in 2003 were dry, with only 137 mm of precipitation during the first five months. During the experiment
and the two weeks preceding it, the weather was warm (with
air temperature up to 29 °C) and dry. The vapor pressure deficit (VPD) reached 2.0–2.3 kPa during the midday hours (Figure 4A). Some clouds occurred during the morning of June 9.
Before application of the localized irrigation, the soil was extremely dry with a mean water content of about 10%vol at a
depth of 35 cm. After irrigation, the soil water content increased to 26% vol in Pit 2, but only in the surface soil layers
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Figure 4. Meteorological conditions during the experiment (A) and
soil water content in three soil pits (B), measured the day after the last
irrigation (see Figure 1 for position of soil pits: 1 = control; 2 = irrigated; and 3 = non-irrigated).
(Figure 4B). The maximum depth to which soil water content
increased after irrigation was 25 cm. The soil water content in
the area between non-irrigated roots (Pit 3) did not change after the application of water and did not appear to differ from
that in the control Pit 1.
Sap flow response to localized irrigation
High heterogeneity of sap flow was recorded in both small and
large roots of the Norway spruce trees before irrigation. Heterogeneity increased after localized application of water. Responses of the examined roots to localized irrigation depended
on their position relative to the irrigated area. This distinction
was made possible following exposure of the whole-root system after the experiment. Roots of two sample trees (Trees 1
and 7) did not reach the watered location. The examined roots
of five other sample trees situated near the watered location
were separated into two main groups: watered and non-watered roots (Table 1).
Responses to localized irrigation in small roots
Four small roots (2w, 2sw, 3w, 6se) extended to the watered location (Figure 1). Root 3w reached the middle of the watered
location and its absorbing watered surface was the highest
when compared to the other small roots (Figure 5A). Sap flow
in this root was close to zero during the night preceding irrigation, but increased rapidly just after irrigation. The nighttime
flow in this root after irrigation was comparable with the daily
maximum values recorded before irrigation. Flow in Root 3w
also increased substantially during the daytime following irrigation, but there was no further response after the second irri-
Figure 5. Sap flow dynamics in the 12 small roots (see Table 1) measured by the single-point sensors. All watered roots (A) demonstrated
increased flow after localized irrigation. Flow in non-watered roots
(B) either decreased to a negative value at night, or the rate of the negative flow recorded before irrigation was reduced following application of water. No responses were recorded in roots of trees distant
from the irrigated location (C). Vertical dashed lines denote periods of
localized irrigation (see Figure 1).
gation. Evidently, this particular root reached its potential absorbing maximum after the first irrigation. The increase in sap
flow in Root 6se following irrigation was also substantial and
this root had the next largest WRAA after Root 3w. Roots 2w
and 2sw of Tree 2 also occurred in the wet soil and showed a
large increase of sap flow in response to the localized irrigation. Sap flow increased more in Root 2w than in Root 2sw
during daytime when water uptake was directly dependent on
the WRAA, which was higher in Root 2w than in Root 2sw.
Sap flow responses to localized irrigation in large roots
Four large roots (2W, 4N, 5NE, 6SE) traversed the watered location (Figure 1). Different rates of increase in sap flow at different xylem depths were observed in large roots. A large
increase in sap flow was recorded in all xylem layers of the
proximal zone of Root 5NE (Figure 6A), which had the highest WRAA. A substantial increase in sap flow was also observed in Root 6SE (Figure 6B), which had a high WRAA,
although lower than that of Root 5NE. However, flow in the
deepest measured xylem layers of Root 6SE did not increase
as substantially as in the outer and the middle xylem layers.
The main part of Root 4N turned sharply to the west when it
was just halfway to the irrigated location, and only four small
surface roots extending in the root’s original direction reached
the edge of the wet area (Figure 1). As a result, an increase in
sap flow was recorded only in the outer xylem of Root 4N
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Figure 6. Sap flow dynamics (left panels) and radial patterns of sap flow
(right panels) measured by multi-point
sensors in large roots that reached the
irrigated location. These roots were arranged (A, B, C, D) from the largest to
the smallest watered-root absorbing areas (WRAA), which were quantified
visually after exposing the roots. The
rate of flow increase depended on
WRAA. Numbers in the legends indicate the depth of the measuring point
below the cambium in mm. Sensors
were installed at similar depths for
roots 5NE, 4N and 2W. The greatest
depth below the cambium is denoted
by the gray area, the shallowest depth
below the cambium is indicated by a
thick black line. Vertical dashed lines
denote periods of localized irrigation
(see Figure 1). Open squares with a
dashed line and filled squares with a
solid line denote day and night radial
pattern of sap flow recorded before irrigation, respectively. Open triangles
with a dashed line and filled triangles
with a solid line denote day and night
radial pattern of sap flow recorded after irrigation, respectively.
(Figure 6C). Only very thin roots of the large Root 2W were
found in the irrigated area, whereas its two largest branches
were directed to the south, almost at right angles to the irrigation location and did not reach the wet soil (Figure 1). The watered absorbing area of Root 2W was smaller than that of Root
4N, which is why only the nighttime increase in sap flow was
detectable in Root 2W and only in the outermost root xylem
layer.
Sap flow in non-irrigated small roots
In contrast to the watered roots, sap flow decreased after irrigation in all of the large and small non-watered roots. The
magnitude and duration of this decrease were dependent on
the position of the non-watered roots relative to the watered
roots and on the amount of available water absorbed by the watered roots from the common wet area that could be redistributed horizontally.
There were five small lateral roots (4n, 4nw, 5ne, 5se and
6ne) that did not reach the irrigated location (Figure 1). Root
5ne was directed away from the wet area, but it was branched
from the watered large Root 5NE. A substantial decrease in
flow to negative values was observed at night in Root 5ne after
both waterings (Figure 5B). No response to irrigation was recorded in Root 5se of the same tree. Root 6ne ramified from
the large non-watered Root 6NE. The magnitude of reverse
flow and duration of the period when it was observed were
lower in the non-irrigated small Root 6ne than in the non-irrigated small Root 5ne. Root 4nw was attached to Root 4NW in
the root proximal zone, close to the stem base. The response of
sap flow to irrigation in Root 4nw was similar to the responses
of the other small roots. The magnitude and longevity of the
reverse night flow recorded in Root 4n before watering decreased when irrigation ceased.
Sap flow in non-irrigated large roots
There were three large roots (4NW, 5SE and 6NE) that did not
pass through the watered area (Figure 1). No response to the
first irrigation was recorded in Root 4NW (Figure 7A). Sap
flow was low in the outer xylem of this root and flow decreased only in the inner xylem after irrigation. As seen after
exposing the roots, Root 5SE was distant from the wet area and
none of its branches was directed there (Figure 1). High nighttime flows were recorded in the deeper xylem of Root 5SE
throughout the experiment (Figure 7B). Evidently, this root
was using water from deeper soil layers through sinker root,
which were found later both close and far from the stem base
(Figures 1 and 3), as found for Australian woody phreatophyte
plants (Dawson and Pate 1996, Burgess et al. 2000b). A detectable decrease in nighttime flow was recorded in the outermost
xylem layers (3 and 13 mm below the cambium) of Root 5SE
after irrigation. Flow decreased in all xylem layers of Root
6NE just after irrigation and its nighttime and daytime values
were significantly lower than before irrigation (Figure 7C). A
substantial decrease in sap flow was recorded in the inner xylem of Root 6NE (cf. sap flow in xylem layers 29 and 11 mm
before and after irrigation). In general, sap flow dynamics in
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NADEZHDINA ET AL.
Figure 7. Sap flow dynamics measured
by multi-point sensors in large roots outside the area of localized irrigation.
These roots were arranged (A, B, C) according to flow response to localized irrigation (from low to high, respectively).
Numbers in legends indicate depth of the
measuring point below the cambium in
mm. The greatest depth below the cambium is denoted by the gray area, the
shallowest depth below the cambium is
indicated by a thick black line. Vertical
dashed lines indicate periods of localized
irrigation (see Figure 1). Open squares
and dotted line and filled squares with a
solid line denote day and night radial
pattern of sap flow recorded before irrigation, respectively. Open triangles with
a dotted line and filled triangles with a
solid line denote day and night radial
pattern of sap flow following irrigation,
respectively.
Root 6NE were similar to those in the small Root 6ne; however, no negative nighttime sap flow was recorded in any xylem layer of Root 6NE.
Sap flow response to localized irrigation in roots of
neighboring trees
The small Root 1w (Figure 5C) did not respond to irrigation.
Its water uptake was characterized by low daytime flows and a
long period of stable reverse flow during the night. The large
Root 1W of this tree did not respond to irrigation either (Figure 8A). Sap flow rates reached their highest values 47 mm below the cambium at night, but during the day the deeper and
shallower xylem layers had comparable values. There was no
response to localized irrigation in any of the measured root
pairs of Tree 7 (Figures 5C, 8B and 8C). Day- and nighttime
values of sap flow at all xylem depths of the large roots, measured at similar evaporative demands, were slightly lower on
the last day of the experiment than on Day 1, indicating decreasing soil water availability. High nighttime sap flows were
recorded in all of these roots.
Discussion
Hydraulic redistribution by roots of Norway spruce trees
Reverse flow is a prerequisite for hydraulic redistribution of
water from wet to dry soil via roots (Burgess et al. 1998,
2000b, 2001b, Caldwell et al. 1998, Brooks et al. 2002, Mor-
Figure 8. Sap flow dynamics measured
by multi-point sensors in large roots of
Trees 1 (A) and 7 (B, C), distant from
the irrigated location. Numbers in legends indicate depth of measuring point
below cambium in mm. The greatest
depth below the cambium is denoted
by the gray area, the shallowest depth
below cambium is indicated by a thick
black line. Vertical dashed lines indicate periods of localized irrigation (see
Figure 1). Open squares with a dotted
line and filled squares with a solid line
denote day and night radial pattern of
sap flow recorded before irrigation, respectively. Gray open triangles with a
dotted line and gray full triangles with
a solid line denote day and night radial
pattern of sap flow recorded after irrigation, respectively.
TREE PHYSIOLOGY VOLUME 26, 2006
HYDRAULIC REDISTRIBUTION BY ROOTS OF NORWAY SPRUCE
eira et al. 2003). There were two small roots in our study (4n
and 1w) that showed evidence of reverse flow at night before
irrigation (Figures 5B and 5C), providing evidence of hydraulic lift by Norway spruce roots. Reverse nighttime sap flow in
Root 4n decreased after watering when the new, more easily
available source of water in the surface soil layers was provided by localized irrigation.
Dry surface soil layers and aboveground plant tissue act as
competing sinks for water lifted hydraulically by deep roots.
The relative strength of these competing sinks determines the
direction and magnitude of the water flow in roots. Large lateral roots serve as conduits, where flows from root branches
are integrated with different rates of loss or uptake (Burgess et
al. 2000b). Unfortunately, there is little published information
on the spatial and temporal radial variations in sap flow in
large lateral roots. Our earlier sap flow measurements in
coarse roots of Norway spruce and lime (Tilia cordata Mill.)
trees (obtained with multi-point sensors) demonstrated that
sap flow in these roots (similar to that in the stem base) was
highly heterogeneous along the xylem radius. Higher flows
typically occurred in the outer sapwood layers, which were
presumably connected with roots in the surface soil horizons
(Nadezhdina and Èermák 2000b). Severing experiments carried out on coarse roots of Norway spruce trees demonstrated
that the conducting function of different sapwood layers in
coarse roots changes in accordance with the variability of their
absorbing conditions (Nadezhdina and Èermák 2000c). The
contrasting sap flow radial patterns at two sensor positions that
were only 40 cm apart on Root 5NE (Figure 3B) could be explained by a large change in root structure along the root close
to the tree base. Many other lateral branches and sinker roots
were connected to this large root along the portion between the
two sensor positions (Figure 3A). Sap flow dynamics at different depths along the root radius at the first sensor position were
typical for dry soil conditions with increasing sap flow toward
the inner xylem (Nadezhdina et al. 2002). High nighttime sap
flow recorded in the deeper sapwood layers may indicate their
connection with sinker roots situated in the deeper (usually
wetter) soil horizons (Nadezhdina et al. 2004b).
Although it is well documented that the outer sapwood contributes more to whole-tree water uptake than inner sapwood
(Dye et al. 1991, Èermák and Nadezhdina 1998, Lu et al.
2000, Delzon et al. 2004), the situation may change when
drought develops in the upper soil, with a relative increase in
the contribution of inner xylem to whole-tree water uptake, as
has been shown for tree stems (Nadezhdina et al. 2002, 2004b,
Ford et al. 2004). Nighttime sap flow was higher in the inner
xylem than in the outer xylem in the majority of large roots examined, reflecting the connection of the inner root conducting
xylem with sinker roots. The preferential use of inner xylem
for root water transport during drought is in agreement with
the widely reported finding that depletion of water stored in
soil proceeds downward as the soils dries (Warren et al. 2005),
allowing high transpiration rates to be maintained in trees
with dimorphic root systems even during dry summer periods
(Meinzer et al. 1999, Irvine et al. 2002).
The reverse (basipetal) nighttime sap flow in the outer xy-
1285
lem layers with opposite acropetal flow in the deeper xylem
layers of the proximal root zone (the second sensor position)
indirectly demonstrated that water from the deeper soil horizons was lifted via sinkers and transferred to superficial neighboring roots through the outer xylem of the proximal zone of
the examined large root. The finding of similar daily values of
sap flow in all xylem layers of Root 5NE at the first sensor position indicates limited water uptake for transpiration, whereas
the similar night values of reverse flow in the outer xylem layers of this root closer to the stem base (the second sensor position) may be explained by the stable soil water potential
difference between wet and dry soil during the night. The
transformation of reverse nighttime sap flows into positive sap
flows in the outer xylem layers of the large Root 5NE immediately after irrigation provides additional evidence of HR before the localized irrigation (Figure 6A). There was no HR in
the absence of gradients of water potentials between deep and
shallow soil layers after irrigation.
Several authors have reported significant nighttime water
uptake during drought. Bucci et al. (2004, 2005) showed that
sap flow continued at night through stems of most common
tropical savanna woody species in central Brazil, and contributed from 13 to 28% of total daily transpiration during the dry
season. Burgess and Dawson (2004) measured nighttime water loss rates of up to 20% of the most rapid summertime transpiration rates. A strong relationship has been found between
VPD and nighttime water loss (Benyon 1999, Burgess and
Dawson 2004). In our Norway spruce trees, the high nighttime
sap flow rates in large roots are indicative of stress conditions
caused by the dry soil (Figures 5 and 6). Nighttime sap flows in
roots were high, even at zero VPD, especially in the watered
roots where nighttime sap flows were higher than the daytime
values recorded before irrigation, reflecting rehydration of
both above- and belowground tree tissues.
Horizontal redistribution of soil water
The extremely fast response of watered roots to irrigation was
accompanied by a decrease in sap flow in non-watered roots at
night. This indicates that water was redistributed horizontally
within root branches of the same root or within different roots
through the stem base. Such movement evidently occurred according to gradients of water potential in the wet and dry
soil and corresponded to the resistances of the particular water pathways. The amounts of transferred water also corresponded well with the WRAA of watered roots connected to
non-watered roots. The amount of transferred water decreased
with increasing distance between the watered and non-watered
roots. Smart et al. (2005) also observed spatially limited water
transfer by roots of grapevines in dry soil, and concluded that
the quantities of water absorbed by roots in the irrigated zone
were sufficient to hydrate only a certain part of the entire root
system. This can also explain why Brooks et al. (2002) detected no reverse sap flow in the root situated on the side of the
plant opposite to that on which water was applied.
We detected no transport of water from irrigated roots via
the soil to roots of neighboring tree, either in small or in large
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NADEZHDINA ET AL.
lateral roots. Localized irrigation had no direct impact on the
water uptake of distant trees. This confirms earlier observations of sap flow responses to localized irrigation in large
beech trees (Èermák et al. 1993) as well as findings of recent
studies on hydraulically lifted water in two common species of
a neotropical savana (Moreira et al. 2003). These authors
found (using the highly sensitive technique of isotopic labeling), that lifted water was utilized by neighboring small shrubs
and trees, but only in small amounts.
Water flow in large roots is more complicated than in small
roots because of the integration of flows from many branches
(Nadezhdina and Èermák 2000b, 2000c). Increased flow after
irrigation, which was higher in the outer xylem than in the inner xylem (e.g., Root 6SE; Figure 6), confirms the link between the outer xylem and superficial roots, where water
uptake was improved by localized irrigation.
Modeling of horizontal water redistribution by roots
Our conceptual model of water uptake provides a basis for interpreting sap flow responses to localized irrigation in Norway
spruce roots. To compare the differences in magnitudes and
rates of responses of different roots, we modeled water uptake
by Norway spruce roots from topsoil based on sap flow in
small roots of Trees 5 and 6. In the model, the two main components of the driving forces for sap flow before irrigation
were the water potentials of the aboveground tissues of the
trees and the water potentials of the soil. For watered roots
having Ψ wet, water potential of the aboveground part of the
tree should equal Ψ dry. According to Equation 3, sap flows in
irrigated roots increased immediately after irrigation in response in sharply increasing A, a difference between Ψ wet and
Ψ dry, and decreasing R. As seen in Figure 5, the magnitude of
the increase in sap flow in roots situated in the same watered
location was dependent on A.
For the non-irrigated roots, a third component of the driving
forces for sap flow appeared after irrigation, namely, the water
potential of the irrigated soil at a point distant from dry roots.
Thus, sap flow in the non-irrigated roots was dependent on
competing sinks represented by the water potentials of the
aboveground portion of the tree and the dry soil relative to the
wet soil. During the night, when needle water potential was
highest, the direction of sap flow reversed because Ψ dry was located in the dry soil rather than aboveground (Figure 9).
Parameter A played an important role as did a new set of resistances in the altered water pathways from the watered roots
through the trunk base or the proximal root zone, to the roots in
the dry soil. The shorter these pathways, the higher the redistributed flow recorded (cf. reverse flow in Roots 5ne and 6ne
in Figure 9). The highest resistance for the movement of hydraulically redistributed water seemed to be located at the stem
base. Resistance R3 for water movement into Root 5se (which
was situated far from the watered area) was evidently higher
than resistances R1 and R2 because no sap flow response to irrigation was recorded in Root 5se.
In general, the probability of detecting nocturnal reverse sap
flow is much higher for small laterals without sinkers. Burgess
et al. (2000b), studying hydraulic redistribution by roots of
Banksia prionotes Lindl., observed evidence of hydraulic redistribution in small (3–5 cm in diameter) laterals, whereas it
was less evident in two big laterals (about 7 cm in diameter).
These authors assumed that measurements of sap flow in the
large “sinker-bearing” laterals integrated varying degrees of
loss or uptake between the superficial and deeply penetrating
parts of the roots (Burgess et al. 2000b). We have presented direct confirmation of such flow integration. The decrease in sap
flow in the large non-watered roots of trees, with access to the
localized irrigation water via other roots, probably occurred
for the following reasons: (1) compensating root rehydration
by both lifted and horizontally redistributed water; and (2) redirection of water from sinkers for rehydration of aboveground tissues of trees. This rehydration seemed more likely to
Figure 9. Hydraulic water redistribution through small and large lateral
roots in a model spruce tree (A) during
a summer drought, when the localized
irrigation was applied (watered zone is
marked by dashed ellipse). Resistances
of pathways for transferred water in
small laterals are marked as R1, R2 and
R3. The root with resistance R1 is attached to a watered root and roots with
resistances R2 and R3 are attached to a
non-irrigated root and differ in distance
from a watered root. Horizontally redistributed flows are shown by dashed
arrows, lifted water in large laterals via
sinkers is marked by thin arrows and
resulting flow in large laterals is
marked by thick arrows. Examples of
sap flow responses in small roots subjected to localized irrigation are shown
in panel B. Abbreviations: Ψ dry_needle =
water potential of dry needles; Ψwet_soil
= water potential of wet soil; and
Ψ dry_soil = water potential of dry soil.
TREE PHYSIOLOGY VOLUME 26, 2006
HYDRAULIC REDISTRIBUTION BY ROOTS OF NORWAY SPRUCE
occur after irrigation through roots that reached the watered
area directly.
Acknowledgments
The work was partially supported by Czech national projects (GACR
No. 522/04/0631, No. 526/02/0792 and MSM 6215648902) and by
the European project “Sustman” (QLK5-CT-2002-00851). We are
grateful to Professor Radomír Ulrich and to Associate Professor
Jindøich Neruda from Mendel University of Agriculture and Forestry
(Brno, CZ) for their support in the field and to Dr. Martin Èermák
from the same university for taking photographic images. Our special
thanks to Dr. Amy Zanne for her valuable help with the first version of
the manuscript and with English corrections.
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