ORIGINAL ARTICLE OA
Functional
Ecology 1999
13, 256–264
000
EN
Reverse flow of sap in tree roots and downward
siphoning of water by Grevillea robusta
D. M. SMITH,* N. A. JACKSON,* J. M. ROBERTS* and C. K. ONG†
*Institute of Hydrology, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK and †International
Centre for Research in Agroforestry, PO Box 30677, Nairobi, Kenya
Summary
1. Constant-power heat-balance sap flow gauges were used to compare sap flow in
vertical and lateral roots of Grevillea robusta trees growing without access to ground
water at a semiarid site in Kenya.
2. Reversal of sap flow occurred when root systems crossed gradients in soil water
potential. Measurement of changes in the direction of flow was possible because of the
symmetrical construction of the sap flow gauges; gradients in temperature across the
gauges, and thus computed rates of sap flow, changed sign when reverse flow occurred.
3. Reverse flow in roots descending vertically from the base of the tree occurred,
while uptake by lateral roots continued, when the top of the soil profile was wetter than
the subsoil. The transfer of water downwards by root systems, from high to low soil
water potential, was termed ‘downward siphoning’; this is the reverse of hydraulic lift.
4. Downward siphoning was induced by the first rain at the end of the dry season and
by irrigation of the soil surface during a dry period.
5. Downward siphoning may be an important component of the soil water balance
where there are large gradients in water potential across root systems, from a wet soil
surface downwards. By transferring water beyond the reach of shallow-rooted neighbours, downward siphoning may enhance the competitiveness of deep-rooted perennials.
Key-words: Agroforestry, hydraulic lift, sap flow gauges, soil water balance
Functional Ecology (1999) 13, 256–264
Introduction
© 1999 British
Ecological Society
There is considerable evidence that water taken up by
plant roots from moist zones of soil can be transported
through the root system and released into drier soil. The
process is thought to be driven passively by gradients in
water potential between zones of soil joined by interconnected roots (Dawson 1993). Most commonly, this
phenomenon has been studied in the context of
‘hydraulic lift’, where water is transferred into dry surface layers of the soil from deeper, wetter subsoil
(Richards & Caldwell 1987; Caldwell & Richards
1989; Dawson 1993), but lateral transport across split
root systems has also been observed (Hansen &
Dickson 1979; Baker & van Bavel 1988). Regardless of
the path of such transport, water must flow away from
the stem in some roots; collectively therefore transport
of water by plant roots from one soil zone to another
can be called ‘reverse flow phenomena’. Here, to
develop further the preliminary report made by Smith,
Jackson & Roberts (1997), we utilize measurements of
reverse flow in tree roots to demonstrate the opposite
process to hydraulic lift: the siphoning of water downwards by root systems of trees spanning the gradient in
water potential between a wet surface and dry subsoil.
Reverse flow phenomena have previously been
investigated using two experimental approaches. In
the first, fluctuations in the water content or potential
of dry soil have been interpreted as the result of the
nocturnal transport of water by roots from adjoining,
more moist soil layers (van Bavel & Baker 1985).
Richards & Caldwell (1987) were thus able to demonstrate in the field that water absorbed at night from
moist soil by deeper roots of the desert shrub
Artemisia tridentata was transported to, and lost from,
roots in drier upper soil layers. Fluctuations in soil
water potential resulted from the subsequent reabsorption of this water during the day for transpiration. Vetterlein & Marschner (1993) similarly found
that water was transferred upwards into dry soil by the
herbaceous root system of Pennisetum americanum.
In the second approach, radioactive or stable isotopes have been used as tracers of soil water movement. Hansen & Dickson (1979) found that 3H2O was
transferred along a series of soil containers interconnected by split root systems. Caldwell & Richards
(1989) fed 2H2O to the distal ends of deep roots of A.
tridentata and found enhanced concentrations of 2H in
neighbouring, shallow-rooted grasses over subsequent
days; concurrent fluctuations in the water potential in
256
257
Reverse flow in
tree roots
the root zone of the grasses indicated that they had
acquired 2H emitted from A. tridentata roots after
hydraulic lift. Dawson (1993) used natural gradients in
2
H/H ratios in soil water to demonstrate hydraulic lift
by roots of Acer saccharum and subsequent uptake by
understorey plants of the water released.
We applied a third technique to the study of reverse
flow phenomena. We used heat-balance sap flow
gauges to distinguish sap flow towards the trunk in
woody roots of Grevillea robusta A. Cunn. from sap
flow in the reverse direction, towards the root tips.
Materials and methods
SITE DESCRIPTION
Measurements of sap flow in roots of G. robusta trees
were made at the Machakos Research Station of the
International Centre for Research in Agroforestry
(ICRAF), Kenya (1° 33 'S, 37° 8 'E; 1560 m above
mean sea level). The site has a semiarid climate, with
mean annual rainfall of 782 mm mostly occurring in
two distinct rainy seasons; mean rainfall from March
to June, the ‘long rains’, is 345 mm; from October to
December, the ‘short rains’, mean rainfall is 265 mm.
The trees were located on a south-facing, 20% slope
with an alfisol (Khandic Rhodustalf), sandy clay loam
in texture, overlying a hard gneiss bedrock at depths
between c. 0·2 and 2·0 m. A water table was not
observed at the site and excavations revealed that the
bedrock was free of deep cracks and that roots of the
trees did not penetrate more than 2–3 mm into the
weathered surface of the rock.
The trees were arranged in a grid pattern with a
3 × 4 m spacing and were 5–6 years old and 8–10 m tall.
The soil beneath the trees was bare and kept weed free.
MEASUREMENT OF SAP FLOW
Of the four widely used techniques for measuring sap
flow in plant stems reviewed by Smith & Allen
(1996), only the heat balance method is suitable for
Fig. 1. Cross-sectional view of a heat-balance sap flow gauge installed on a root,
showing the symmetrical arrangement of the thermocouple junctions used to measure
the gradients in temperature across the heater, ∆Ta and ∆Tb; when the direction of
flow is reversed, the mean temperature gradient (∆T) changes sign.
use on roots if sap flow can reverse direction. The
symmetrical design of heat-balance sap flow gauges
(Fig. 1) means that, when used with a constant power
supply, output from the gauge simply changes sign if
the direction of flow is reversed. When used with conventional, assymetric configurations of sensors, the
heat-pulse or thermal-dissipation methods would fail
if flow reversed direction, although modifications to
the heat-pulse method can be made to enable measurement of flow in either direction (S. Burgess,
unpublished data). The heat balance method would be
similarly inappropriate for use on roots if used with a
variable power supply that is regulated to maintain a
constant temperature gradient across the gauge
(Ishida, Campbell & Calissendorf 1991), as the power
supply would merely increase if flow reversed, in an
attempt to re-establish the temperature gradient.
When constant-power sap flow gauges are used, the
circumference of a short, insulated section of stem or
root is heated with an electric heater. The power supplied to the heater, output from a radial thermopile and
the gradients in temperature across the heater, ∆Ta and
∆Tb (Fig. 1), are used to quantify components of the heat
balance of the gauge; the residual of the heat balance is
the heat absorbed by the moving sap stream (qf). The
mass rate of sap flow (F) is finally calculated from qf
and the mean change in temperature across the heater
(∆T) using (Sakuratani 1981; Baker & van Bavel 1987):
qf
F = ––––– ,
cs ∆T
eqn 1
where cs is the specific heat capacity of sap and
∆T = (∆Ta + ∆Tb)/2.
DATA COLLECTION
Constant-power sap flow gauges were installed on
roots after excavating around trees up to c. 0·4 m from
the base of the trunk. Roots that were of a suitable size
and sufficiently straight to accommodate a sap flow
gauge were then selected and excavations extended as
required. Soil was removed to a depth of 0·2 m around
lateral roots and a depth of 0·4 m around vertical roots.
Installations were made during three periods; a
description of the roots and sizes of gauge used in
each case are listed in Table 1. Installation 1 was made
between 26 November and 17 December 1996.
Rainfall ceased for the season on 29 November, when
the seasonal total had reached only 157 mm.
Installation 2 was made on roots of a second tree
between 21 March and 15 April 1997, enabling
changes in the dynamics of sap flow associated with
the onset of rains to be recorded, as the dry season
ended with 50 mm of rain on 30 March. The final
period, Installation 3, was between 13 June and 1 July
1997, when gauges were installed on roots of a third
tree. This period occurred after the end of the long
rains, but 45 mm of irrigation was applied to a 6 × 8 m
area centred on the tree between 23 and 25 June.
258
D. M. Smith et al.
Table 1. Roots for which sap flow was measured during three periods of observation. The nominal diameter of the gauge used
and the diameter of the root at the mid-point of the gauge are given, with the cross-sectional area (Ax) of each root at the base of
the trunk and the summed Ax of all vertical or lateral roots of each tree
Installation
Root description
1
near-surface lateral
vertical
near-surface lateral
vertical
near-surface lateral
subsurface lateral, descending at 15°
from horizontal, 0·3 m below
surface
vertical
2
3
Shelters constructed from polythene prevented rain
flooding the excavations and diverted stemflow away
from the exposed roots. To minimize the influence of
fluctuations in ambient conditions on the performance
of the gauges, black netting was suspended over the
shelter, shading the gauges from direct sunlight, and
sections of roots left exposed after installation of the
gauges were insulated with foam pipe lagging and
covered with aluminium foil. With these precautions,
problems identified by Lott et al. (1996) with the use
of sap flow gauges on roots were not encountered.
Output from the gauges was recorded using an
AM416 multiplexer and 21X data logger (Campbell
Scientific Ltd, Shepshed, UK); measurements were
made every 30 s and logged as 10 min averages. The
temperature of the heated section of root was measured
in all cases by placing a 0·2 mm-diameter copper-constantan thermocouple junction beneath the heater. This
temperature was used to estimate a storage term in the
heat balance of the gauge (Smith & Allen 1996).
SETTING OF K SH
To deduce radial heat fluxes from sap flow gauges,
and thus enable determination of qf, a constant representing the thermal conductance of the gauge, often
called the sheath conductance (Ksh), must be evaluated for each new installation. When gauges are used
on stems, Ksh is commonly calculated using data from
predawn periods when it can be assumed there is no
sap flow (Smith & Allen 1996); however, when sap
flow in both directions along a root is suspected this
assumption cannot be made. As a consequence, values
of Ksh for the gauges installed on roots were determined from data collected at the end of each period of
measurement, after sap flow was stopped by severing
the root below the distal end of the gauge.
Gauge diameter
(mm)
Root diameter
(mm)
Ax
(cm2)
Total Ax
(cm2)
25
16
19
25
16
30
15
17
28
18
12·9
5·7
4·4
13·6
5·5
57·0
38·8
101·9
63·0
162·0
25
19
29
22
7·9
3·4
9·4
70·4
(IH II, Didcot Instrument Co., Abingdon, UK) and
45 mm-diameter aluminium access tubes, which had
been in place since 1993. For Installation 1, these
measurements were made in a plot with a similar soil
depth and the same configuration of trees, c. 80 m
from the tree instrumented with sap flow gauges. For
Installations 2 and 3, measurements were made using
access tubes 1·0 and 1·8 m upslope from the base of
the instrumented trees; these tubes were situated
beyond the influence of the shelters covering the
excavated roots. Readings were taken regularly at
depth increments of 0·2 m, between 0·2 m and the
underlying bedrock.
For Installations 1 and 2, water potentials were calculated from measured soil water contents using water
retention curves for the five soil horizons identified at
the site. Pressure plate apparatus was used to determine the retention characteristics of undisturbed cores
from each horizon and parameters of the retention
curves were fitted by regression (Campbell 1985). The
appropriate retention curve for each depth increment
of each access tube was selected by identifying the
extent of the different horizons in each profile; this was
accomplished using results from particle size analyses
of samples extracted during installation of the access
tubes. For Installation 3, soil water potentials between
the depths of 0·1 m and the bedrock were measured
every 0·1 m using an array of tensiometers located 1 m
upslope from the trunk of the tree.
During Installations 1 and 3, a pressure chamber
was used to measure the water potentials of leaves
from the crowns of the instrumented trees.
Measurements were made at regular intervals between
the predawn period and sunset on several days; mean
leaf water potentials were determined from a minimum of three leaves at each time interval.
Data analysis
DETERMINATIONS OF SOIL AND LEAF WATER
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
POTENTIALS
Profiles of soil water content were measured over
each period of observation using a neutron probe
Equation 1 shows that when ∆T is zero or close to zero,
F is undefined or implausibly high. For this reason, it is
recommended that the power supplied to gauges is set
so that, even at the highest rates of flow, ∆T is always
259
Reverse flow in
tree roots
higher than about 1·0 °C. When the direction of flow
reverses, however, ∆T must pass through zero, causing
values of F calculated with equation 1 to become undefined. Thus, if flow in roots reversed direction, it was
necessary to filter out data from the transition period
when calculated flow rates became excessive.
Examination of the sap flow data collected revealed
that the period of transition in the direction of flow
could be distinguished on the basis of two criteria that
were met concurrently only during a change in the
direction of flow: F was set to zero if ∆T  ≤ 2·0°C
and (∆Tb – ∆Ta) ≥ 1·0 °C. The latter criterion was
effective because it was not met when flow rates were
truly high, as (∆Tb – ∆Ta) is proportional to the conductive heat flux from the gauge (Smith & Allen
1996), which is always low when sap flow is rapid.
Results and discussion
MEASUREMENT OF FLOW REVERSAL
The performance of a constant-power sap flow
gauge during the reversal of flow in a vertical root is
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
Fig. 2. Data from a sap flow gauge, installed on a vertical
root of Grevillea robusta, recorded on 13 December 1996:
(a) (∆Tb – ∆Ta) and ∆T , where ∆T = (∆Ta + ∆Tb)/2; (b) the
ratio of heat absorbed by the moving sap stream (qf) to the
power supplied to the gauge heater (P); (c) rates of sap flow,
before and after filtering of data from the period of transition
between positive and negative flow, where positive flow was
towards the trunk.
shown in Fig. 2. The key to identifying periods of
reverse flow was the sign of ∆T (Fig. 2a), which was
positive when sap warmed by the heater moved
towards the trunk, but negative when sap flowed in
the opposite direction, towards the root tips. Uptake
of heat by the moving sap stream was substantial
during both day and night (Fig. 2b), except during
transitions between positive and negative flow. Flow
was thus measured in both directions, although the
filtering out of unreliable data near transition periods
resulted in the loss of some resolution in rates of sap
flow at these times (Fig. 2c).
SAP FLOW IN ROOTS AFTER A POOR RAINY SEASON
The record of sap flow in roots from Installation 1 is
shown in Fig. 3. For the entire period of observation,
sap flow in the lateral root was positive, indicating
uptake of water from the soil. Uptake continued at
substantial rates throughout each night, although nocturnal flow rates declined as the period progressed. In
the vertical root, sap flow was negative, or towards the
root tips for much of the period. Rates of reverse flow
were highest at night and declined as positive flow
rates in the lateral root peaked during the day. Later,
overnight rates of downward flow in the vertical root
gradually declined and, after 11 December, sap flow
became positive during the middle of the day.
All lateral roots of the tree were severed on 15
December. The high rates of sap flow recorded in the
lateral root on this day were probably the result of
increased uptake compensating for the severing of other
roots (Lott et al. 1996), as the gauged lateral was the last
to be cut. The following day, sap flow was far higher in
the vertical root than on previous days, with much lower
rates of downward flow overnight; severing of the laterals thus forced uptake through the vertical roots of the
tree. This response to the cutting of roots confirmed that
the sap flow gauges were operating correctly.
Figure 4 shows profiles in soil water potential (ψs)
during Installation 1. At the start of the period, because
the rains had been insufficient to wet the whole profile,
there was a strong gradient in ψs between the wet surface and drier soil below 0·4 m. Thus, the downward
flow of water observed in the vertical root appears to
have resulted from the transfer of water, after uptake
by lateral roots, along a gradient in ψs between the surface layer and drier soil at the bottom of the profile.
This is the process of downward siphoning of water by
roots, the opposite of hydraulic lift.
Downward siphoning of water at night was apparently supplied by nocturnal uptake of water by lateral
roots, although some of this uptake may have re-filled
storage capacity in the trunk. Prior to 6 December,
downward siphoning continued throughout the day,
indicating that a proportion of the transpiration stream
was diverted down into vertical roots. The decline in
reverse flow in the vertical root over subsequent days
and nights occurred as the surface dried after rainfall
SAP FLOW IN ROOTS AFTER IRRIGATION OF THE SOIL
260
D. M. Smith et al.
SURFACE
Prior to the application of irrigation during
Installation 3, there was uptake of water by each of the
gauged roots during the day, but no measurable sap
movement at night (Fig. 7). Wetting of the soil by irrigation was mostly confined to the top 0·3 m of the
profile (Fig. 8) and the gradient in ψs created was
small, because soil below this level had retained considerable amounts of water after the recently concluded long rains. The gradient in ψs was, however,
sufficient to induce changes in the pattern of sap
movement: during the nocturnal periods following
irrigation, uptake of water by the near-surface lateral
continued and sap flow was negative in both the subsurface lateral and the vertical roots. Wetting of the
top of the soil profile thus caused downward siphoning of water by the tree, although the rates of downward flow were low because the gradient in soil water
potential was small.
Fig. 3. Sap flow in (a) a 30 mm-diameter lateral root of
Grevillea robusta and (b) a 15 mm-diameter vertical root
during Installation 1; positive flow was towards the trunk.
All lateral roots of the tree were cut on 15 December.
ceased on 29 November and the subsurface layers
became wetter, causing the gradient in ψs to gradually
weaken (Fig. 4).
SAP FLOW IN ROOTS AT THE ONSET OF THE RAINY
SEASON
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
The effects of the first rains at the end of the dry season on sap flow in a G. robusta root system are shown
in Fig. 5. Before the storm on 30 March, rates of sap
flow were low in both the vertical and lateral root,
with higher uptake by the vertical root, probably
because most soil water was available from between
the depths of 0·6 and 1·2 m (Fig. 6). Within c. 12 h of
the initial wetting of the soil surface by rain, which
began near midday on 30 March, these patterns of sap
movement changed markedly. Uptake of water by the
lateral root increased rapidly, quickly exhibiting the
same pattern of sap flow seen in the lateral root during
Installation 1; rates of sap flow peaked during the day
but uptake continued throughout the night. In the vertical root, sap flow reversed direction during the night,
although negative flow always ceased during the day.
Thus, when the first rains after a long dry period
wetted the soil surface and created a vertical gradient in ψs (Fig. 6), the root system of the tree quickly
began siphoning water downwards from the surface.
The gradient in ψs was about one order of magnitude smaller than during Installation 1, however,
and so rates of downward flow in the vertical root
were lower in this instance and reverse flow did not
continue during the day.
WATER RELATIONS OF DOWNWARD SIPHONING
The occurrence of reverse flow in vertical roots may
depend on the water potential in xylem at the base of
the trunk (ψb), where horizontal and vertical roots
meet. Sap flowing towards the trunk in horizontal roots
would then be diverted downwards and result in reverse
flow whenever ψb remained higher than the potential of
water at the tips of the vertical roots, which would be
approximately equal to the potential of surrounding
soil. The highest values of ψb would have occurred
overnight, when transpiration was negligible and leaf
water potentials (ψl) approached their predawn maxima. Thus, the gradient in potential across the vertical
roots would tend to have been largest at night, resulting
in the highest rates of downward flow.
Fig. 4. Profiles of total soil water potential (ψs) on 28
▲) and 12 December (●)
November (■), 5 December (▲
1996, during Installation 1.
was – 0·2 ± 0·7 MPa, which was lower than ψs at any
depth (Fig. 8). Despite this, small downward flows
were recorded during the night in the vertical root and
the subsurface lateral. Rather than suggesting countergradient transport of water in the tree, however, the
disparities in ψl and ψs most probably resulted from
imprecision in the determination of ψl, heterogeneity
in ψs and the height of the crown above the soil, which
at c. 10 m would account for a potential difference of
0·1 MPa; ψb was probably intermediate to ψs near lateral and vertical roots, resulting in a gradient in potential (Fig. 8) sufficient to drive downward siphoning.
261
Reverse flow in
tree roots
FATE OF WATER SIPHONED DOWNWARDS
Fig. 5. Sap flow in (a) a 17 mm-diameter lateral and (b) a
28 mm-diameter vertical root of Grevillea robusta during
Installation 2; positive flow was towards the trunk. Rainfall
over the period is shown in (c).
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
Prior to 2 December 1996, during Installation 1, the
minimum ψl recorded in the middle of the day was
– 1·0 ± 0·07 MPa. Heterogeneity in soil water distribution near the trees may have caused variation in the gradient in ψs with depth, but such a decline in ψl over the
day was probably not sufficient to overcome the gradient in ψs below 0·4 m (Fig. 4) and induce water uptake
from these depths. However, ψb must have declined
with ψl, causing the gradient in water potential across
the vertical root to diminish during the day, when the
tree was transpiring rapidly; hence, diversion of the
transpiration stream downwards continued throughout
the day, but the rate of reverse flow in the vertical root
was lower during the day than at night (Fig. 3).
Later in the first period of observation, on 14
December, the minimum ψl measured was
– 1·3 ± 0·2 MPa, which was probably low enough for
uptake of water to occur from the bottom of the profile (Fig. 4); sap flow in the vertical root was consequently positive during the middle of the day (Fig. 3).
As ψl increased overnight to the predawn maximum
of – 0·4 ± 0·01 MPa, concurrent increases in water
potential in lateral roots and in ψb would have reestablished the downward gradient in potential
across the root system, so that flow in vertical roots
was negative at night (Fig. 3).
The water relations of downward siphoning during
Installation 3 are less clear, as the mean predawn ψl
Reverse flow in roots does not appear to result in equilibration of water potentials across root systems and
therefore the gradual elimination of such flow. The
continual downward flow of water observed in the
vertical root over many days during the initial period
of Installation 1 suggests that water passed from the
roots into the rhizosphere, as storage of such quantities of water in root tissue without rapid equilibration
of water potentials does not seem possible. Wetting of
the rhizosphere could ultimately have the same effect,
because the low hydraulic conductivity of the drier
bulk soil would slow the diffusion of water away from
the root, causing the water potential in the rhizosphere
to increase and rates of reverse flow in roots to
decrease. However, when rates of reverse flow were
highest, during nocturnal periods, they were nearly
constant, with no indication that reverse flow slowed
as nights progressed.
Emission of water from roots may not therefore
have been limited by the conductivity of the sandyclay-loam textured soil at this site. In addition, some
water may have been emitted into predominantly dry
Fig. 6. Profiles of total soil water potential (ψs) on 27
March (■), 31 March (▲
▲), 6 April (●) and 9 April (◆
◆) 1997,
during Installation 2.
262
D. M. Smith et al.
downward siphoning on soil water balances, sap flow
must be measured in more roots of each tree than was
possible in this study. The observed rates of downward
flow in roots indicate, however, that downward siphoning may be a substantial component of the soil water
balance where vertical gradients in soil water potential
are large. Emerman & Dawson (1996) reached a similar conclusion for hydraulic lift, as they estimated that
c. 20% of daily uptake by an A. saccharum tree was
transferred to surface soil layers by reverse flow.
ECOLOGICAL IMPLICATIONS OF DOWNWARD
SIPHONING
Fig. 7. Sap flow in (a) an 18 mm-diameter near-surface lateral, (b) a 29 mm-diameter subsurface lateral and (c) a
22 mm-diameter vertical root of Grevillea robusta during
Installation 3; positive flow was towards the trunk. Irrigation
was applied to the soil surface during the period indicated by
the shaded region of the x-axis.
soil, a possibility if emission was only from the tips of
growing roots, as Jensen, Sterling & Wiebe (1961)
observed when dye was used to trace the path of water
drawn by suction in the reverse direction through solution-grown plants. Consequently, some water transported by reverse flow may be utilized in cell expansion
and to wet the rhizosphere near root tips and thus ease
the passage of growing roots through dry soil. A
question for future research is, therefore: does reverse
flow in roots support root growth into dry soil?
Downward siphoning may have important consequences for interactions between trees and neighbouring, understorey plants with shallower root systems.
Emission of water into soil may result in the storage of
water, if it can be re-extracted at a later time, below
the maximum rooting depth of neighbours. Storage of
water in this way could increase the efficiency of
water utilization by trees, as it could reduce the
amount of water lost by evaporation from the soil, and
reduce the availability of water to shallow-rooted
neighbours. Downward siphoning of water could
therefore give trees a competitive advantage over
neighbours in dry environments where plants are
reliant on seasonal rainfall for water.
If downward siphoning supports root growth, it may
enable trees to maintain a network of deep roots during
periods when seasonal rains are poor and only wet the
surface layer of the soil. Such growth, which need only
be sufficient to replace fine roots lost as a result of natural turnover, would enable trees to rapidly exploit water
from below the root zone of shallow-rooted neighbours
during seasons wet enough to recharge subsurface soil
layers, thus ensuring the trees have a larger resource
pool than neighbours and so a competitive advantage.
EFFECTS OF DOWNWARD SIPHONING ON THE SOIL
WATER BALANCE
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
Approximation of rates of sap flow in whole root systems can be attempted by extrapolating from sap flow
in single roots on the basis of the cross-sectional area
of roots at the base of the trunk. When sap flow measured in Installation 1 was extrapolated to the whole
root system on this basis, using root cross-sectional
areas in Table 1, the mean proportion of water taken
up by lateral roots each day that was diverted downwards into vertical roots was 0·26. During
Installations 2 and 3, rates of flow in vertical roots
were lower and so this fraction was smaller.
Such estimates likely contain large uncertainties,
however, because of variation in the lengths of each
major root exposed to different water potentials in each
soil layer. Thus, to properly quantify the influence of
Fig. 8. Profiles of total soil water potential (ψs) on 18 June
(■), 26 June (▲
▲) and 29 June (●) 1997, during Installation 3.
263
Reverse flow in
tree roots
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
At sites in arid or semiarid regions where deeprooted trees or shrubs utilize ground water, downward
siphoning may enable roots to grow down through dry
soil layers to the water table. Downward siphoning
may therefore be an important adaptation allowing
juvenile phreatophytic plants to make the transition
from reliance on seasonal rainfall to exploitation of
ground water.
Like downward siphoning, hydraulic lift has implications for resource utilization and interactions
among coexisting species. Hydraulic lift is hypothesized to have a role in facilitating the acquisition of
nutrients from dry, but fertile, surface soils, by mobilizing nutrient ions and prolonging the activity of soil
micro-organisms (Caldwell, Richards & Beyschlag
1991). As the availability of nutrients from deeper
soils is typically low, hydraulic lift may consequently
play a key role in maintaining the nutritional health of
deep-rooted plants in dry regions. Downward siphoning is unlikely to have a similar function, however,
because it occurs when the soil is wettest near the surface, so that uptake of nutrients is not limited by
water availability.
Caldwell et al. (1991) suggested that, like downward siphoning, hydraulic lift enables plants to store
water for later use, when transpirational demand cannot be met by the sparse root network in the subsoil. In
contrast to downward siphoning, however, hydraulic
lift also makes water available to shallow-rooted
neighbours (Corak, Blevins & Pallardy 1987;
Caldwell & Richards 1989; Dawson 1993), creating a
form of parasitism in which water resources captured
by one species are transferred to competitors
(Caldwell et al. 1991). While downward siphoning
may enhance the competitiveness of deep-rooted trees
and shrubs, the opposite process, hydraulic lift, may
therefore improve the competitive ability of neighbours; thus, hydraulic lift may encourage close spatial
relations between trees and grasses in water-limited
environments, while downward siphoning encourages
their separation.
Reverse flow phenomena hold similar ramifications
for the design and management of agricultural systems which combine species, such as agroforestry.
Storage of water through downward siphoning would
enhance the competitiveness of trees, by transferring
resources away from zones that are accessible to
crops. Downward siphoning would therefore tend to
reduce the extent to which the patterns of water uptake
by crops and trees such as G. robusta are thought to be
complementary (Lott et al. 1996; Howard et al. 1997).
The competitiveness of trees would, in contrast, be
reduced by hydraulic lift, if it enhanced the availability of water to crops (Emerman & Dawson 1996).
Thus, while hydraulic lift might allow a higher density
of trees to be grown without deleterious effects on
crops, it could be necessary, for example, to increase
the spacing between trees in agroforestry in conditions where downward siphoning may be substantial.
Conclusions
Downward siphoning may be an important, though
previously missing, component of the soil water balance at locations where gradients in water potential
across root systems, from a wet soil surface downwards, are large. These conditions are most likely to
be found in arid or semiarid regions where there is no
water table or only a very deep water table. Vertical
gradients in water potential at such sites are probably
largest, and therefore downward siphoning most
important, when seasonal rains are poor, as was the
case in this study during Installation 1, or when rainstorms bring an end to long dry spells, as occurred
during Installation 2.
By transferring water beyond the reach of more
shallow-rooted neighbours, downward siphoning by
deep-rooted perennials may have a significant impact
on the distribution of vegetation and interactions
among species in natural ecosystems, such as savannas or desert-shrub communities. Downward siphoning is also likely to influence the partitioning of water
resources between trees and crops in agroforestry; at
sites where considerable downward siphoning is possible therefore this should be reflected in the strategies
used to design and manage agroforestry systems.
Constant-power sap flow gauges provide an important new tool for the investigation of downward
siphoning and reverse flow phenomena in general.
They will enable hydraulic lift and downward siphoning to be quantified in the field, and when combined
with measurement of soil water and the use of isotopic
tracers, they will enable study of the role of reverse
flow phenomena in resource acquisition strategies
used by plants.
Acknowledgements
This publication is an output from a research project
funded by the Department for International
Development of the United Kingdom. However, the
Department for International Development can accept
no responsibility for any information provided or
views expressed. The work described here was funded
from project R6363 of the Forestry Research
Programme. We are especially grateful for the able
technical assistance given by staff at Machakos
Research Station, in particular Mr Elijah Kamalu and
Mr Patrick Angala. We also thank Dr Simon Allen for
valuable advice given during the planning and implementation of this study.
References
Baker, J.M. & van Bavel, C.H.M. (1987) An analysis of the
steady-state heat balance method for measuring sap flow
in plants. Plant, Cell and Environment 10, 777–782.
Baker, J.M. & van Bavel, C.H.M. (1988) Water transfer
through cotton plants connecting soil regions of differing
water potential. Agronomy Journal 80, 993–997.
264
D. M. Smith et al.
© 1999 British
Ecological Society,
Functional Ecology,
13, 256–264
van Bavel, C.H.M. & Baker, J.M. (1985) Water transfer by
plant roots from wet to dry soil. Naturwissenschaften 72,
606–707.
Caldwell, M.M. & Richards, J.H. (1989) Hydraulic lift:
water efflux from upper roots improves effectiveness of
water uptake by deep roots. Oecologia 79, 1–5.
Caldwell, M.M., Richards, J.H. & Beyschlag, W. (1991)
Hydraulic lift: ecological implications of water efflux
from roots. Plant Root Growth: an Ecological
Perspective (ed. D. Atkinson), pp. 423–443. Blackwell
Scientific Publications, Oxford.
Campbell, G.S. (1985) Soil Physics with BASIC. Elsevier,
Science Publishing., Amsterdam.
Corak, S.J., Blevins, D.G. & Pallardy, S.G. (1987) Water
transfer in an alfalfa/maize association. Plant Physiology
84, 582–586.
Dawson, T.E. (1993) Hydraulic lift and water use by plants:
implications for water balance, performance and
plant–plant interactions. Oecologia 95, 565–574.
Emerman, S.H. & Dawson, T.E. (1996) Hydraulic lift and its
influence on the water content of the rhizosphere: an
example from sugar maple, Acer saccharum. Oecologia
108, 273–278.
Hansen, E.A. & Dickson, R.E. (1979) Water and mineral
nutrient transfer between root systems of juvenile
Populus. Forest Science 25, 247–252.
Howard, S.B., Ong, C.K., Black, C.R. & Khan, A.A.H.
(1997) Using sap flow gauges to quantify water uptake by
tree roots from beneath the crop rooting zone in agroforestry systems. Agroforestry Systems 35, 15–29.
Ishida, T., Campbell, G.S. & Calissendorf, C. (1991)
Improved heat balance method for determining sap flow
rate. Agricultural and Forest Meteorology 56, 35–48.
Jensen, R.D., Sterling, A.T. & Wiebe, H.H. (1961) Negative
transport and resistance to water flow through plants.
Plant Physiology 36, 633–638.
Lott, J.E., Khan, A.A.H., Ong, C.K. & Black, C.R. (1996)
Sap flow measurements of lateral tree roots in agroforestry systems. Tree Physiology 16, 995–1001.
Richards, J.H. & Caldwell, M.M. (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by
Artemisia tridentata roots. Oecologia 73, 486–489.
Sakuratani, T. (1981) A heat balance method for measuring
water flux in the stem of intact plants. Journal of
Agricultural Meteorology 37, 9–17.
Smith, D.M. & Allen, S.J. (1996) Measurement of sap flow in
plant stems. Journal of Experimental Botany 47, 1833–1844.
Smith, D.M., Jackson, N.A. & Roberts, J.M. (1997) A new
direction in hydraulic lift: can tree roots siphon water
downwards? Agroforestry Forum 8 (1), 23–26.
Vetterlein, D. & Marschner, H. (1993) Use of a microtensiometer technique to study hydraulic lift in a sandy
soil planted with pearl millet (Pennisetum americanum
[L.] Leeke). Plant and Soil 149, 275–282.
Received 13 March 1998; accepted 7 July 1998