Blackwell Science, LtdOxford, UK
PCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2001
25
796
Interactions between elevated CO2 and drought
S. D. Wullschleger et al.
Original ArticleBEES SGML
Plant, Cell and Environment (2002) 25, 319–331
Plant water relations at elevated CO2 – implications for
water-limited environments
S. D. WULLSCHLEGER, T. J. TSCHAPLINSKI & R. J. NORBY
Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6422, USA
ABSTRACT
Long-term exposure of plants to elevated [CO2] leads to a
number of growth and physiological effects, many of which
are interpreted in the context of ameliorating the negative
impacts of drought. However, despite considerable study, a
clear picture in terms of the influence of elevated [CO2] on
plant water relations and the role that these effects play in
determining the response of plants to elevated [CO2] under
water-limited conditions has been slow to emerge. In this
paper, four areas of research are examined that represent
critical, yet uncertain, themes related to the response of
plants to elevated [CO2] and drought. These include (1)
fine-root proliferation and implications for whole-plant
water uptake; (2) enhanced water-use efficiency and consequences for drought tolerance; (3) reductions in stomatal
conductance and impacts on leaf water potential; and (4)
solute accumulation, osmotic adjustment and dehydration
tolerance of leaves. A survey of the literature indicates that
the growth of plants at elevated [CO2] can lead to conditions whereby plants maintain higher (less negative) leaf
water potentials. The mechanisms that contribute to this
effect are not fully known, although CO2-induced reductions in stomatal conductance, increases in whole-plant
hydraulic conductance and osmotic adjustment may be
important. Less understood are the interactive effects of
elevated [CO2] and drought on fine-root production and
water-use efficiency, and the contribution of these processes
to plant growth in water-limited environments. Increases in
water-use efficiency and reductions in water use can contribute to enhanced soil water content under elevated
[CO2]. Herbaceous crops and grasslands are most responsive in this regard. The conservation of soil water at elevated [CO2] in other systems has been less studied, but in
terms of maintaining growth or carbon gain during drought,
the benefits of CO2-induced improvements in soil water
content appear relatively minor. Nonetheless, because even
small effects of elevated [CO2] on plant and soil water relations can have important implications for ecosystems, we
conclude that this area of research deserves continued
investigation. Future studies that focus on cellular mechanisms of plant response to elevated [CO2] and drought are
needed, as are whole-plant investigations that emphasize
the integration of processes throughout the soil–plant–
atmosphere continuum. We suggest that the hydraulic prinCorrespondence: Stan D. Wullschleger. Fax: +1 865 576 9939;
e-mail: [email protected]
© 2002 Blackwell Science Ltd
ciples that govern water transport provide an integrating
framework that would allow CO2-induced changes in stomatal conductance, leaf water potential, root growth and
other processes to be uniquely evaluated within the context
of whole-plant hydraulic conductance and water transport
efficiency.
Key-words: Atmospheric CO2 enrichment; carbon
allocation; global change; osmotic adjustment; osmotic
potential; stomatal conductance; transpiration; water-use
efficiency; water stress.
INTRODUCTION
Exposing plants to long-term CO2 enrichment invariably
leads to a range of growth and physiological responses
(Mousseau & Saugier 1992; Norby et al. 1999; Pritchard &
Rogers 2000). In general, elevated [CO2] increases plant
biomass, root mass and total leaf area (Rogers, Runion &
Krupa 1994; Curtis & Wang 1998) and alters leaf net
photosynthetic rates, stomatal conductance and water-use
efficiency (WUE) (Gunderson & Wullschleger 1994; Saxe,
Ellsworth & Heath 1998). Although these growth and
physiological effects can be considerable, there is evidence
that the magnitude of such responses is dependent on the
availability of other potentially limiting resources (Chaves
& Pereira 1992; Morison 1993; Campbell, Stafford Smith &
McKeon 1997). Soil resources, such as nitrogen, and environmental variables, such as light and temperature, are all
significant in this respect (Long 1991; Field, Jackson &
Mooney 1992; Stitt & Krapp 1999). However, for the vast
majority of terrestrial ecosystems, water is considered the
primary factor limiting growth and productivity (Schulze et
al. 1987) and thus, the interaction between elevated [CO2]
and soil water is an important scientific issue with relevance to both the basic plant sciences and global change
research.
Many studies have addressed the interactions that arise
between elevated [CO2] and drought, and most have
focused on one or more components of plant water
relations (Morse et al. 1993; Tschaplinski, Norby &
Wullschleger 1993; Centritto et al. 1999b; Ellsworth 1999;
Tognetti, Raschi & Jones 2000a). A few studies have
addressed the potential interaction between elevated [CO2]
and drought by direct multifactor manipulations (Johnsen
1993; Centritto, Lee & Jarvis 1999a; De Luis, Irigoyen &
Sanchez-Diaz 1999), whereas others have taken a more
319
320 S. D. Wullschleger et al.
observational approach by comparing drought-induced
changes in plant water relations at natural CO2 springs
(Tognetti et al. 1999a) or inferring CO2–drought interactions by observing seasonal patterns of response (Ellsworth
1999). Regardless of how such studies are conducted, there
has long been the temptation to interpret results in the
context of the potential ameliorating effects that elevated
[CO2] may have on the drought response of plants.
Increased allocation of carbon to root growth and osmotic
adjustment in plants exposed to elevated [CO2] may, for
example, ameliorate the negative impacts of water stress by
improving the capacity to extract soil water, whereas CO2induced reductions in stomatal conductance may ameliorate drought by increasing leaf or whole-plant WUE, thus
enabling plants to better exploit water-limited environments. Elevated [CO2] may also influence water relations
and plant responses to drought by altering developmental
processes, including root and shoot architecture (Berntson
& Woodward 1992; Miao, Wayne & Bazzaz 1992) and leaf
morphology (Thomas & Harvey 1983). However, despite
these interpretations, there are few examples illustrating
the effects of elevated [CO2] on plant water relations and,
in turn, the significance of these effects to plant and/or ecosystem productivity under water-limited conditions. One
notable exception is that of Owensby and colleagues who
have successfully used a combination of approaches (measurements of leaf water potential to whole-ecosystem gas
exchange) to show that reduced water use in a C4 tallgrass
prairie exposed to elevated [CO2] was sufficient to increase
above- and below-ground biomass production in years
when water stress was frequent (Knapp, Hamerlynck &
Owensby 1993; Ham, Owensby & Coyne 1995; Owensby
et al. 1997).
Because significant interactions do occur between elevated [CO2] and drought, and because many effects of plant
water relations have important implications for ecosystems
in water-limited environments, we feel that this area of
research deserves continued investigation. Therefore, in
this paper, we examine four topics of plant water relations
research that represent critical, yet uncertain, themes
related to the response of plants to elevated [CO2] under
water-limited conditions. These topics span a range of scales
from cellular to whole plant and encompass a diversity of
processes from CO2-induced increases in solute accumulation and osmotic adjustment of leaves, to the enhanced production of fine roots in plants grown at elevated [CO2] and
implications for whole-plant water use. Our primary focus
is on the response of woody perennials to elevated [CO2]
and drought, but where appropriate, we also consider how
these responses relate to other studies with herbaceous
crops and grassland species. The interactions that arise from
a combination of atmospheric CO2 and drought are complex and we note that a clear picture has been slow to
emerge from the many studies conducted in the area of
plant water relations. We discuss what might be contributing to this unfortunate lack of scientific certainty and make
recommendations whereby additional insights might be
derived from future investigations.
FINE-ROOT PROLIFERATION AND
IMPLICATIONS FOR WHOLE-PLANT WATER
UPTAKE
Increases in fine root production under elevated CO2
represent yet another mechanism whereby forests
might adjust to future climates. If greater rooting density and/or depth is attained by forests in the future they
may be able to tap new water sources and maintain
normal function under altered atmospheric conditions.
(Hanson & Weltzin 2000)
In his review, Morison (1993) observed that greater carbon
allocation to roots as a mechanism to improve plant water
status at elevated [CO2] was an attractive teleonomic argument, but cautioned that such an effect lacked consistent
experimental evidence. From a historical perspective, there
have been many observations that root systems become
larger when plants are grown in CO2-enriched atmospheres, dating back to some of the earliest experiments
with potted plants in growth chambers. For example, wheat
(Triticum aestivum L.) plants grown in deep pots in growth
cabinets with different levels of soil moisture displayed
increases in root weight in response to elevated [CO2]
under dry conditions only (Gifford 1979). Moreover,
growth of white oak (Quercus alba L.) seedlings in nutrientpoor soil increased in elevated [CO2], with the dry mass of
tap roots increasing 93% and that of fine roots increasing
111% (Norby, O’Neill & Luxmoore 1986). Responses such
as these were recognized almost immediately to be a potentially important determinant of how plants respond to
drought under field conditions, especially if increased
growth at elevated [CO2] allowed roots to gain access to
deeper layers of soils and associated soil water.
If plants grow larger overall at elevated compared to
ambient [CO2], root mass can logically be expected to
increase as well. To consider whether there is a specific
CO2-induced stimulation of root growth, i.e. whether dry
matter distribution is affected by elevated [CO2], many
researchers have considered the response of the root-toshoot ratio (R/S). Stulen & den Hertog (1993) pointed out
that many experimental problems exist with this statistic,
but nevertheless concluded that although R/S is not
influenced by elevated [CO2] when water and nutrients
are non-limiting, it is increased by elevated [CO2] when soil
resources are limiting, as was the case with the wheat and
white oak examples cited earlier. A thorough compilation
of the literature, however, does not support a general effect
of elevated [CO2] on R/S (Norby 1994). When differences
in R/S are noted between CO2 treatments, they often are
associated with an effect of [CO2] on plant ontogeny. That
is, plants grow faster in elevated [CO2], and R/S changes
during plant development. When viewed allometrically,
few effects of elevated [CO2] on dry matter allocation have
been observed (Norby 1994; Tissue, Thomas & Strain
1997).
The capacity of the root system to take up water
depends not on root mass, but on rooting volume (or rooting depth) and fine-root area and activity. The size of root
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Interactions between elevated CO2 and drought 321
systems of white oak seedlings was significantly stimulated
by elevated [CO2] in a growth chamber experiment (Norby
et al. 1986), although there was no significant difference in
whole-plant water use between treatments over a 40 week
period. In a subsequent experiment with the same species
(Norby & O’Neill 1989), root growth was not increased in
elevated [CO2] and water use was lower than in seedlings
grown in ambient air. In both cases, whole-plant WUE
increased significantly in elevated [CO2], but in neither of
these experiments were the plants subjected to drought.
Thus, the importance of the increased WUE to drought tolerance or avoidance cannot be evaluated. Increases in the
size of root systems were observed with CO2 enrichment in
five studies of intact native grasslands, but no significant
increases occurred in seven others (Arnone et al. 2000).
King, Thomas & Strain (1997) observed increased root surface area in Pinus taeda (loblolly pine) and P. ponderosa
(Ponderosa pine) seedlings in elevated [CO2], which was
entirely attributable to whole-plant growth, not a redistribution of biomass. Increased fine root production and seasonal increases in fine root standing crop have also been
observed in forest stands exposed to elevated [CO2]
(Norby & Jackson 2000; Matamala & Schlesinger 2000).
However, in none of these cases has the increased fine root
production been associated with increased water uptake.
Indeed, water uptake is more likely to be reduced because
of elevated CO2 effects on canopy transpiration
(Wullschleger & Norby 2001).
Atmospheric CO2 enrichment can change the distribution of roots in the soil, which might also have implications
for water uptake. Fine roots at the soil surface may be beneficial in capturing water after a dry soil is rewetted (Kosola
& Eissenstat 1994). Several experiments suggest that crop
plants in a higher CO2 atmosphere will have larger root systems that are more highly branched, especially at shallow
depths, and this should increase the capacity for resource
acquisition, but at lower efficiency (Pritchard & Rogers
2000). CO2 enrichment of a grassland community led to an
upward shift in root length density with a greater proportion of roots in the top 6 cm soil layer (Arnone et al. 2000).
This shift was perhaps related to increased soil moisture
and its effect on nutrient availability. In a sandy, nutrientpoor, oak-palmetto system, CO2 enrichment stimulated
root production both near the surface, where nutrient availability was greatest, and at greater depth, where water was
most available (Day et al. 1996).
To relate the size of the root system more closely to
water balance, it is reasonable to consider the ratio of fineroot mass (length or area would be better) to leaf area (FR/
LA); that is, the balance between the supply organ and the
demand organ. The FR/LA of yellow-poplar (Liriodendron
tulipifera L.) seedlings increased in elevated [CO2], and this
response was interpreted as a compensatory response that
increased whole-plant WUE through morphological adjustments rather than through stomatal adjustments (Norby &
O’Neill 1991). In six CO2 enrichment experiments with
deciduous trees in the field, FR/LA increased in elevated
[CO2] (Norby et al. 1999). However, Tingey, Phillips &
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Johnson (2000) concluded that there was no consistent
effect of elevated [CO2] on FR/LA in conifers.
Although it is reasonable to speculate that an increase
in FR/LA increases the capacity of a plant to maintain a
favourable water balance, there are no field observations
that directly support this hypothesis. Why is this? In pot
studies, effects of elevated [CO2] on water use can often be
explained simply by differences in the amount of leaf area.
In field experiments as well, effects of elevated [CO2] on
water balance will be manifested primarily through effects
on leaf area and canopy conductance. Describing a CO2
effect on water uptake related to root deployment requires
separating out numerous confounding influences and system feedbacks. When soil moisture is adequate to meet
transpirational losses, CO2 effects on root volume are presumably irrelevant, so detection of this mechanism would
be possible only under specific conditions. Reduced canopy
transpiration in high [CO2] could reduce root uptake of
water regardless of a prior effect on root volume, and this
could result in increased soil moisture (Hungate et al. 1997)
and secondary effects on root growth. The response of fineroot production to changes in soil moisture varies considerably in different experiments and may be confounded by
concurrent changes in N availability (Joslin, Wolfe &
Hanson 2000). Any interactions between CO2 and water
via root activity might be swamped by interactions between
CO2 and N or some other soil resource.
Much of the focus of investigations of root system
responses to CO2 enrichment has been toward long-term
changes that might affect carbon flux to soil or plant-soil N
dynamics. Short-term changes may be more important in
consideration of water balance. An acceleration of root
growth in elevated [CO2] could result in a seedling becoming established more rapidly and avoiding water deficits.
Polley et al. (1996) observed this in an experiment with
Prosopis glandulosa (honey mesquite) seedlings. Low
water availability restricts the establishment of this invasive
shrub in some grasslands. Root growth in their experiment
was stimulated by CO2 enrichment, a response that Polley
et al. (1996) observed as an increase in the ratios of lateral
root to total root mass and lateral root mass to leaf area.
Seedling survival during drought was significantly higher,
and the authors attributed this to a combination of reduced
water use per leaf and an increase in potential water uptake
per leaf following from the higher ratio of lateral root to
leaf area. Additional observations by Tischler et al. (cited in
Polley et al. 1996) showed that CO2 enrichment increased
rooting depth of mesquite seedlings, and that the rapid
establishment of deep roots effectively uncoupled the shrub
from competition for water with more shallow-rooting
grasses. Similarly, Tolley & Strain (1984) speculated that
since CO2 enrichment increased the R/S ratio of sweetgum
(Liquidambar styraciflua L.) more than loblolly pine,
sweetgum would become more competitive and better able
to become established in drier areas currently dominated
by pine seedlings. Jifon, Friend & Berrang (1995) studied
the competitive interactions of these two species under elevated [CO2] and concluded that resource-rich soil con-
322 S. D. Wullschleger et al.
ditions enhanced the CO2–induced stimulation of soil
colonization by sweetgum roots in sweetgum-pine mixtures.
In conclusion, the premise that increased root growth of
plants in elevated [CO2] will increase water uptake,
improve water balance, or help to avoid water deficits may
be well founded, but it has not yet been well supported with
experimental data. The extent to which such mechanisms
operate in nature and their biological significance must be
evaluated in the context of other effects of elevated [CO2],
interacting environmental influences, and internal and system-level feedbacks. As a result, observations that support
the importance of root proliferation to whole-plant water
uptake are likely to remain anecdotal.
spheric CO2 enrichment, primarily as a result of reduced
stomatal conductance, enhanced photosynthesis, or both
factors in combination (Eamus 1991; Drake, GonzàlezMeler & Long 1997; Saxe et al. 1998). Increases in ITE due
to elevated [CO2] range from 25 to 229% (average 93%
over 13 studies) and represent probably the most consistent
and responsive measure in CO2 effects research (Saxe et al.
1998). However, leaf-level measurements of ITE are hard
to interpret in the context of plant water relations, and few
mechanistic insights about the response of whole plants to
elevated [CO2] are conveyed by this simple metric (Jarvis,
Mansfield & Davies 1999). Total leaf area per plant, shoot
and root hydraulic conductance, above- and below-ground
allocation of biomass and the duration of leaf area development can all be important in determining water use and,
hence, the drought tolerance of a species, yet these properties are not reflected in ITE. A more meaningful, albeit less
reported, measurement of plant response to elevated [CO2]
is WUE or the amount of total biomass produced per unit
water used (Eamus 1991). Although conceptually similar to
ITE, the term WUE conveys a more integrated measure of
plant response to elevated [CO2].
A sampling of recent literature indicates that wholeplant WUE, like that observed for ITE, increases considerably with elevated [CO2] (Table 1). Calculated increases in
WUE range from no effect in the case of a well-watered
ENHANCED WATER-USE EFFICIENCY
AND CONSEQUENCES FOR DROUGHT
TOLERANCE
It is sometimes assumed that because increases in
atmospheric CO2 concentrations usually enhance
water use efficiency per unit leaf area, there will be a
tendency for plants to show greater drought
tolerance . . . in the future. (Beerling et al. 1996)
Many studies have shown an increase in instantaneous transpiration efficiency (ITE) for leaves exposed to atmo-
Species
Conditions
Change
in WUE
(%)
Arrhenatherum elatius
GH, Watered
GH, Stressed
GH, Watered
GH, Stressed
GH, Watered
GH, Stressed
OTC, High water
OTC, Med water
OTC, Low water
OTC, High water
OTC, Med water
OTC, Low water
FACE
GC, Watered
GC, Stressed
GH, Watered
GH, Stressed
SPAR, Flooded
SPAR, Reflooded
SPAR, Droughted
OTC, Watered
OTC, Stressed
OTC, Watered
OTC, Stressed
GH, Watered
GH, Stressed
OTC
GH, Watered
GH, Stressed
+30
+45
+18
+38
+31
+33
+27
+43
+51
−1
+22
+16
+28
+180
+150
+29
+36
+41
+39
+125
+47
+52
+47
+18
+39
+50
+36
+36
+47
Calluna vulgaris
Erica tetralix
Grassland – Sandstone
Grassland – Serpentine
Liquidambar styraciflua
Medicago sativa
Molinia caerulea
Oryza sativa
Prunus avium
Quercus robur
Rumex obtusifolius
Tallgrass prairie
Vaccinium myrtillus
Reference
Arp et al. 1998
Arp et al. 1998
Arp et al. 1998
Table 1. Whole-plant, stand or ecosystem
water-use efficiency (WUE) expressed as a
percentage change with atmospheric CO2
enrichment. Plants were exposed to elevated
[CO2] either in growth chambers (GC), soil–
plant–atmosphere-research (SPAR)
chambers, greenhouse (GH), open-top
chambers (OTC) or free-air CO2
enrichment (FACE) facilities
Field et al. 1997
Field et al. 1997
Wullschleger & Norby 2001
De Luis et al. 1999
Arp et al. 1998
Baker et al. 1997b
Centritto et al. 1999a
Picon et al. 1996
Arp et al. 1998
Owensby et al. 1997
Arp et al. 1998
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Interactions between elevated CO2 and drought 323
serpentine grassland (Field et al. 1997) to 180% increase in
WUE for a study in which potted alfalfa (Medicago sativa
L.) was exposed to elevated [CO2] and a 15 d drought (De
Luis et al. 1999). The majority of values, however, fall within
the range of 30–50% and, in general, the impact of elevated
[CO2] on WUE appears greater in plants and ecosystems
under drought conditions (Field et al. 1997; Arp et al. 1998).
The period of time over which the studies summarized in
Table 1 assessed WUE varied from daily to seasonal. In one
of the longer studies to date, Wullschleger & Norby (2001)
reported that WUE for 12-year-old sweetgum trees
exposed to free-air CO2 enrichment (FACE) for a 7 month
growing season was 1·90 g of woody biomass produced per
kilogram water used compared to 1·48 g kg−1 for trees in the
ambient CO2 treatment. This 28% increase in stand-level
WUE was the combined result of a 15% increase in dry
matter increment (Norby et al. 2001) and a 12% decrease in
stand water use (as measured by sap flow techniques).
Although our discussion has thus far dealt with CO2induced effects on ITE and WUE, it should be emphasized
that the total amount of water used by plants, stands and
ecosystems exposed to elevated [CO2] and drought is also
of much interest. An increase in WUE per se does not
ensure that water use on an individual plant basis will be
Water loss (kg d-1)
2·0
(a)
1·5
1·0
0·5
Water-use efficiency (g kg-1)
0.0
(b)
25
20
15
10
5
0
69–80
69–90
69–103 69–115
Days after emergence
Figure 1. Total water loss (a) and plant water-use efficiency (b)
of droughted cherry seedlings grown in ambient (cross-hatched)
and elevated (open) [CO2], during the first-growing season
drought cycle. Data are the means of three plants per treatment ±1
SE. Letters (a, b) indicate significant differences at P < 0·05.
Modified from Centritto et al. (1999a).
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
less or, in turn, that soil moisture will be different between
CO2 treatments. Centritto et al. (1999a) observed in
droughted cherry (Prunus avium L.) seedlings that
although whole-plant WUE increased 56–103% with elevated CO2 (Fig. 1b), there were no effects of CO2 on water
use (Fig. 1a). Picon, Guehl & Aussenac (1996) observed an
increase in WUE for well-watered (47%) and droughted
(18%) Quercus robur L. seedlings exposed to atmospheric
CO2 enrichment, but noted that whole-plant water use was
similar between the two CO2 treatments. It should be
emphasized that in both of these studies, a lack of effect on
total water use occurred because leaf area was higher in
plants grown at elevated [CO2], which emphasizes the overriding importance of plant and canopy development in
determining responses observed in many CO2 enrichment
studies with young trees.
Equivalent rates of water use for plants exposed to
ambient and elevated [CO2] suggest that there are important trade-offs between increases in leaf area and reductions in stomatal conductance, such that in many cases there
are few, if any, effects of elevated [CO2] on whole-plant
water use. One question that needs to be asked in this
regard is how much of an increase in leaf area per plant (or
LAI for a stand or ecosystem) is required to balance a CO2induced reduction in stomatal conductance? The answer to
this question is dependent on the initial leaf area (closedcanopy versus isolated plants) and the extent to which canopy transpiration is under stomatal control. For example, in
canopies with high LAI, leaf boundary layer and aerodynamic conductance may exert a stronger control on water
vapour exchange than stomatal conductance, so that any
change in stomatal conductance induced by elevated [CO2]
may only marginally affect transpiration and hence, plant
and stand water use. Niklaus, Spinnler & Körner (1998)
reported that ecosystem-level controls of the water balance
(soil moisture, leaf area) can, in responsive systems like
grasslands, far outweigh the physiological effects of elevated [CO2] observed at the leaf level.
In comparison with studies that report limited or no
effect of elevated [CO2] on whole-plant water use, some
studies have shown that water use in highly responsive
plants and ecosystems may be considerably lower at elevated, compared to ambient, [CO2] (Field et al. 1997;
Owensby et al. 1997; Niklaus et al. 1998). Field et al. (1997)
estimated that water savings in serpentine grasslands
exposed to elevated [CO2] reached maximum values of 0·3–
0·4 mm d−1 in each of three water treatments, whereas in
sandstone grasslands a marked 2·15 mm d−1 decrease in
evapotranspiration (ET) due to CO2 enrichment was
observed. Integrated over the season, these CO2-induced
reductions in ET led to cumulative savings of water under
elevated [CO2] that ranged from 23 to 87 mm, depending
on watering regime. One important consequence of these
effects of elevated [CO2] on water use should be a conservation of soil moisture and, thus, soil water content in plots
exposed to elevated [CO2] should be generally higher than
under ambient conditions. In the sandstone grasslands, elevated [CO2] led to increased soil moisture during at least
324 S. D. Wullschleger et al.
Figure 2. Soil water content for a nutrient-poor calcareous
grassland in north-western Switzerland exposed to ambient (open)
and elevated (cross-hatched) [CO2]. Soil water content in the 0–10cm depth was measured gravimetrically in each of 16 field plots;
error bars indicate standard errors. * P ≤ 0·05, ** P ≤ 0·001.
Modified from Niklaus et al. (1998).
part of the growing season (Field et al. 1997). Niklaus et al.
(1998) also observed such a response in calcareous grasslands and concluded that non-significant responses of water
loss (i.e. transpiration) to elevated CO2 as measured by gas
exchange accumulated over time and resulted in significantly higher soil moisture in CO2-enriched plots (Fig. 2).
Few studies have quantitatively evaluated the significance of these soil moisture effects on plant growth and/or
physiology during drought. Higher soil water contents in
elevated, compared to ambient, CO2 treatments might convey a margin of drought tolerance to plants and ecosystems
if that conserved water were available to either postpone
the onset or severity of drought. In the study reported by
Baker et al. (1997a), CO2 enrichment of rice (Oryza sativa
L.) reduced daily water use by 5–10% and during a 20 d
drought cycle this conserved water allowed 1–2 d more
growth. Based on our calculations, using data in Baker et al.
(1997a), an extension of the photosynthetic period by a few
days would amount to an additional daytime CO2 uptake of
approximately 1·5 mol CO2 m−2 compared to a 20 d uptake
of 15 mol CO2 m−2 or about a 10% increase in net daytime
carbon uptake. In the study of Niklaus et al. (1998) the
water conserved at elevated [CO2] was, according to the
authors, sufficient to explain a 20% increase in aboveground biomass due to conservation of soil water alone.
Other studies have indicated that reduced water use by
plants at elevated [CO2] was sufficient to extend the photosynthetically active period when water became limiting in
the ecosystem (Owensby et al. 1997), but this particular
study did not quantify the magnitude of the response.
Wullschleger & Norby (2001) reported a 20 mm difference
in water use during the month of May for a sweetgum stand
exposed to elevated [CO2] and we calculate, using a WUE
of 1·90 g biomass produced per kilogram water consumed,
that this would lead to an additional 38 g biomass produced
per square metre ground area if indeed this conserved
water were available for growth. Such an increase in the
production of biomass due to water conservation alone represents 4·1% of the annual biomass increment for trees in
the elevated CO2 treatment.
Our analysis suggests that although ITE and WUE are
often reported to increase in response to elevated [CO2], it
is difficult to separate CO2-induced effects on photosynthesis and growth from those on leaf transpiration and wholeplant water. As a result, these metrics convey only limited
mechanistic information on the response of plants to atmospheric CO2 enrichment. More important is whether plants
and ecosystems exposed to elevated [CO2] conserve soil
water compared to ambient [CO2]. Unfortunately, few
studies actually quantify the magnitude of water conserved
at elevated [CO2] and still fewer consider how this conservation of soil water may potentially impact plant growth
and physiology in water-limited environments. For those
studies that do characterize the significance of reduced
water use at elevated [CO2] in terms of maintaining growth
or carbon gain during drought, the benefits of CO2-induced
improvements in soil water content appear minor. Nonetheless, even small changes in soil water content can be
important to nitrogen mineralization, organic matter
decomposition and the survival of young plants in areas
where periodic droughts are frequent. Thus, CO2 enrichment studies that link plant and soil-based processes
should be encouraged.
REDUCTIONS IN STOMATAL
CONDUCTANCE AND IMPACTS ON LEAF
WATER POTENTIAL
Elevated [CO2], by causing a decline in stomatal
conductance, might reduce transpiration rate, leading
to an increase in plant water potential and a delay in
the onset of drought . . . Moreover, it is reasonable to
suppose that less negative plant water potentials in
drying soils enable plants to remain turgid and
functional for longer. (Centritto et al. 1999b)
A common expectation from many, albeit not all, studies
that address the physiological response of plants to elevated [CO2] is that stomatal conductance will be reduced.
In herbaceous species, these reductions can approach 27–
40% (Morison 1985; Field et al. 1995), whereas in some
coniferous species the response may be considerably less
(Teskey 1995; Tissue et al. 1997; Ellsworth 1999). Nonetheless, this response has long fuelled the debate as to whether
CO2-induced reductions in stomatal conductance will be of
sufficient magnitude to impact leaf water potentials, particularly during periods of water-deficit stress. Moreover, if
significant effects on plant water relations are observed,
what then will be the consequences of this to leaf, plant and
ecosystem function?
Attempts to address the influence of elevated [CO2] on
plant water relations have now spanned almost 25 years
(Cure & Acock 1986; Lawlor & Mitchell 1991). Early studies, conducted mostly with agricultural crops, showed
marked responses of leaf water potential to elevated [CO2]
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Interactions between elevated CO2 and drought 325
(Rogers et al. 1984; Bhattacharya et al. 1990; Prior et al.
1991; Allen et al. 1994) and significant interactions between
atmospheric CO2 and drought have been observed (Bhattacharya et al. 1990; Prior et al. 1991). Leaf water potentials
in soybean (Glycine max L.) exposed to elevated [CO2]
during a 4 d drought were more than 0·5 MPa higher (less
negative) than those from plants exposed to ambient [CO2],
with the greatest effects observed during the latter stages of
an imposed water stress period (Rogers et al. 1984). At the
time these studies were conducted, a typical conclusion was
that elevated [CO2] ameliorated, mitigated or compensated
for the negative impact of drought on plant growth. Indeed,
Rogers et al. (1984) concluded that even though greater
growth and leaf area production were observed at high
atmospheric [CO2], lower rates of water use in soybean
delayed the onset of severe water stress under conditions of
low soil moisture. More recently, however, quantifying the
long-term effects of elevated [CO2] and drought on plant
water relations has been recognized as problematic given
complications that arise from increases in whole-plant leaf
area, effects of elevated [CO2] on plant ontogeny (Centritto
et al. 1999a), difficulties associated with maintaining similar
soil moisture levels among plants with different rates of soil
water extraction (De Luis et al. 1999), species differences
(Ferris & Taylor 1995) and day-to-day variation in radiation, vapour pressure deficit and precipitation.
Notwithstanding these difficulties, a number of studies
have indicated that elevated [CO2] can lead to conditions
whereby plants maintain higher (less negative) leaf water
potentials. A survey of the literature published in the past
decade (1990–2000) shows that there have been repeated
attempts to examine the impact of elevated [CO2] on one or
more aspects of plant water relations, including measures of
leaf water and/or turgor potential (Table 2). Many of these
Table 2. Literature survey on the influence of elevated [CO2] either alone or in combination with drought on leaf water potential and turgor
potential. Plants were grown either in growth chambers (GC), soil-plant-atmosphere-research (SPAR) chambers, greenhouse (GH), opentop chambers (OTC), free-air CO2 enrichment (FACE) facilities or natural CO2 springs
Species
Conditions
Water
potential
Abutilon theophrasti
Amaranthus hypochondriacus
Andropogon gerardii
Anthyllis vulneraria
Avena barbata
Erica arborea
GH
GH
OTC
GC
OTC
CO2 Spring
+
+
+
o
+
+
Glycine max
OTC, Watered
OTC, Stressed
SPAR, Watered
SPAR, Stressed
GC
OTC
OTC, Watered
OTC, Stressed
CO2 Spring
o
+
+
+
+
+
o
+
+
GH
GC, Watered
GC, Stressed
CO2 Spring
o
o
–
+
GC
GC, Watered
GC, Stressed
FACE
GH
GH
OTC, Watered
OTC, Stressed
CO2 Spring
CO2 Spring
GC
GC
GH
+
+
+
o
o
+
o
–
o
+
+
o
–
Grassland spp.
Ipomoea batatas
Juniperus communis
Lotus corniculatus
Medicago sativa
Myrtus communis
Panicum coloratum
Picea mariana
Pinus taeda
Plantago media
Prosopis glandulosa
Prunus avium
Quercus ilex
Quercus pubescens
Quercus robur
Sanguisorba minor
Zea mays
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Turgor
potential
+
+
o
+
+
+
o
Reference
Bunce & Ziska 1998
Bunce & Ziska 1998
Owensby et al. 1993
Ferris & Taylor 1994
Jackson et al. 1994
Tognetti et al. 2000a
Tognetti et al. 2000b
Prior et al. 1991
Allen et al. 1994
Allen et al. 1998
Field et al. 1997
Bhattacharya et al. 1990
Tognetti et al. 2000a
Tognetti et al. 2000b
Ferris & Taylor 1994
De Luis et al. 1999
+
Tognetti et al. 2000a
Tognetti et al. 2000b
Seneweera, Ghannoum & Conroy 1998
Johnsen 1993
o
o
Ellsworth 1999
Ferris & Taylor 1994
Polley et al. 1996
Centritto et al. 1999b
o
Tognetti et al. 1998
Tognetti et al. 1999a
Schulte et al. 1998
Ferris & Taylor 1994
Bunce & Ziska 1998
326 S. D. Wullschleger et al.
studies were conducted under field conditions using opentop chambers (OTC), free-air CO2 enrichment (FACE)
technology or natural CO2 springs, with a few explicitly
considering the potential interaction of elevated [CO2] and
drought. A brief examination of Table 2 shows that plant
growth at elevated [CO2] can, as suggested by earlier investigations, lead to higher leaf water and turgor potentials.
Tognetti et al. (2000b) recently conducted a comprehensive
examination of plant water relations for three Mediterranean shrubs (Erica arborea L., Myrtus communis L. and
Juniperus communis L.) growing at a natural CO2-emitting
vent near Laiatico, Italy. It was observed that differences in
leaf conductance between CO2 vent and control sites were,
over an annual cycle, significant for all three species, with
plants at the CO2 vent showing lower leaf conductances
than plants at the control site. These changes were accompanied by small, but highly significant effects on leaf water
potential (Fig. 3). In the plants growing near the CO2 vent,
both pre-dawn and midday water potentials were higher
0
(a)
-1
Midday water potential (MPa)
-2
-3
-4
(b)
-1
-2
-3
-4
(c)
-1
-2
-3
-4
Month (1996–1997)
Figure 3. Seasonal course of midday shoot water potential
measured in the sun crown of (a) Erica arborea (b) Myrtus
communis and (c) Juniperus communis plants at a CO2 spring site
(closed symbols) and at the control site (open symbols) from
October 1996 to September 1997. Modified from Tognetti et al.
(2000b).
(less negative) than those at the control site, and differences were most pronounced between July and September
when drought was severe (soil water content approaching
12%). Tognetti et al. (2000b) interpreted these data to indicate that plants growing near the CO2 vent were either conserving soil water due to direct effects of elevated [CO2] on
leaf conductance or that they had improved access to soil
water due to a deeper root system. All three species maintained higher turgor potentials under elevated [CO2] during
a mid-season drought (Tognetti et al. 2000a).
Not all studies have shown a clear distinction between
CO2 treatments in terms of plant water relations (Table 2).
Tognetti et al. (1998), in an analysis of Quercus ilex at a natural CO2 spring in central Italy, observed that elevated
[CO2] decreased leaf conductance, sap flux density and
whole-plant hydraulic resistance, but exerted no effect on
leaf water potential. A similar lack of response in leaf water
potential to elevated [CO2] was observed by Ferris & Taylor
(1994) and Ellsworth (1999), albeit in the latter study with
loblolly pine, a significant response might not have been
expected given that no effect of atmospheric [CO2] on stomatal conductance was observed. Although it is not surprising that some studies report no effect of elevated [CO2] on
leaf water potential, it is interesting that a few recent studies have shown that leaf water potentials may actually be
lower (more negative) in plants grown at elevated [CO2]
(Centritto et al. 1999b; De Luis et al. 1999). The mechanisms
that contribute to these effects are not known. Increases in
whole-plant leaf area beyond that which can be compensated for by CO2-induced reductions in stomatal conductance may lead to greater rates of soil drying and associated
plant water stress. There is also evidence that during
drought, stomatal conductance in some species may be
higher (not lower) in elevated [CO2] (Heath & Kerstiens
1997). This creates a condition whereby soils at elevated
[CO2] become drier and plants are subjected to a higher
severity of drought. Heath & Kerstien (1997) observed in
beech (Fagus sylvatica L.) that stomatal conductance during drought was higher at elevated compared to ambient
[CO2] and that this resulted in a substantially greater rate of
soil drying for plants exposed to atmospheric CO2 enrichment. The explanation for this response was that wholeplant water relations at elevated [CO2] were improved,
either through more effective uptake of water by the roots
or through increased xylem conductivity at elevated [CO2],
which would improve the supply of water to the leaves during periods of high evaporative demand. The consequence
of fine-root proliferation to plant water relations in plants
exposed to elevated [CO2] and drought has already been
discussed. On the other hand, hydraulic conductance of
intact plants grown at ambient and elevated [CO2] has been
determined, but unfortunately the response has been highly
variable. Increases, decreases and no change in leaf-specific
hydraulic conductance with elevated [CO2] have been
observed (Bunce 1996; Bunce & Ziska 1998; Tognetti et al.
1998; Tognetti et al. 1999b). Regardless of the mechanisms
involved, rising [CO2] cannot be assumed to improve the
water economy of all plant species, and in some cases there
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
Interactions between elevated CO2 and drought 327
may be deleterious effects (Beerling et al. 1996; Robinson,
Heath & Mansfield 1998).
Finally, studies that report positive effects of elevated
[CO2] on leaf water and turgor potentials have not adequately addressed the question as to the growth and/or
physiological benefits derived from these responses. Tognetti et al. (2000a) proposed that since Mediterranean
shrubs maintained higher turgor potentials under elevated
[CO2], the growth of these species in water-limited environments should be impacted less than plants exposed to
drought under ambient [CO2]. However, the causal relationships among effects on leaf water potential, turgor
potential and maintenance of growth at elevated [CO2]
have seldom been quantified. Ferris & Taylor (1994) tried
to demonstrate cause-and-effect relationships among leaf
water potential, turgor potential, cell wall elasticity and rate
of leaf and leaflet extension in four chalk grassland species
exposed to CO2 enrichment, but were unable to identify
any single relationship to explain their observations.
SOLUTE ACCUMULATION, OSMOTIC
ADJUSTMENT AND DEHYDRATION
TOLERANCE
In addition to effects of elevated CO2 on plant-water
relations that are mediated by stomata, other response
mechanisms can be considered. For instance . . .
Elevated CO2 may also directly alter leaf dehydration
tolerance in cases where CO2-induced excess carbohydrates serve as osmotica. (Ellsworth 1999)
Hypothetically, elevated [CO2] could increase drought tolerance of plants if increased rates of net carbon assimilation
lead to an increased availability of substrate for osmotic
adjustment, thereby lowering osmotic potential at full turgor (πo). Elevated [CO2] could therefore have a significant
effect on drought tolerance by inducing carbohydrate accumulation and lowering πo when soil moisture availability is
high, as well as by enhancing osmotic adjustment during
drought. Morse et al. (1993) reported a decline in πo of
0·11 MPa in gray birch (Betula populifolia Marsh.) with elevated [CO2] under mesic conditions. Furthermore, for this
same species, a 0·14 MPa osmotic adjustment to xeric conditions under ambient CO2 increased to a 0·2 MPa adjustment under elevated [CO2]. Ferris & Taylor (1994) reported
that three of the four chalk grassland herbs that they studied, including salad burnet (Sanguisorba minor Scop.), kidney vetch (Anthyllis vulneraria L.) and hoary plantain
(Plantago media L.), had lower foliar osmotic potentials (by
0·3 MPa) when grown at elevated compared to ambient
[CO2]. These authors considered the possibility that the
slow growth rate of these herbaceous species may have permitted solute accumulation under atmospheric CO2 enrichment. Similarly, in a study where there was no growth
response to elevated [CO2] and seedlings were subjected to
a drought late in the growing season, Vivin et al. (1996)
reported that leaf πo of Quercus robur seedlings was
reduced by 0·4 MPa in elevated, but not ambient [CO2].
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 319–331
However, an osmotic adjustment of 0·3 MPa in roots
exposed to drought was not affected by CO2 enrichment.
Although Picon, Ferhi & Guehl (1997) did not determine
osmotic potential at full turgor, they reported that a
drought-induced increase in hexose concentrations was
more pronounced under elevated [CO2]. Again, the lack of
sink activity under drought probably led to the modest
increase. They noted that only plants from the elevated CO2
treatment had a fourth growth flush, indicating high sink
activity. When growth stimulation was evident, carbohydrate accumulation was not observed, and there were only
slight increases in sucrose and starch concentrations. Therefore, πo may decrease in response to elevated [CO2] if sink
demand for soluble carbohydrates is low.
In contrast, elevated [CO2] could have no effect or even
decrease dehydration tolerance if growth promotion
depletes the concentrations of organic solutes, such as soluble carbohydrates, phenolic compounds and organic acids,
which can be particularly low in rapidly growing seedlings
(Tschaplinski & Blake 1989). Leaf πo and osmotic adjustment were not affected by elevated [CO2] in sugar maple
(Acer saccharum L.), American sycamore (Platanus occidentalis L.) and sweetgum, where, despite an approximate
50% increase in net carbon assimilation rate (Tschaplinski
et al. 1995b), there was no evidence of higher soluble carbohydrate concentrations in leaves or roots (Tschaplinski,
Stewart & Norby 1995a). The rapid growth response of
seedlings to elevated [CO2] may depress solute concentrations in leaves, increasing πo and lowering drought tolerance. This tendency was exhibited by loblolly pine seedlings
grown in elevated [CO2], where πo of needles increased by
0·08 MPa in well-watered seedlings and by 0·16 MPa in
stressed seedlings, suggesting that drought tolerance of
shoots may have been somewhat less at elevated [CO2]
(Tschaplinski et al. 1993). This was offset, however, by an
increase in the soluble carbohydrate concentrations in
roots of seedlings grown under elevated [CO2], which
can potentially facilitate continued water uptake under
drought. In well-watered seedlings, elevated [CO2]
increased the concentration of soluble carbohydrates in
roots by 68% (Tschaplinski et al. 1993). Water stress
reduced the soluble carbohydrate concentrations in roots
of seedlings growing in ambient [CO2] to 26% that of the
well-watered controls. Elevated [CO2] mitigated the water
stress-induced decline in soluble carbohydrate concentrations in roots, perhaps due to carbohydrate loading when
the seedlings were growing under conditions of higher
water supply, rather than to osmotic adjustment to water
stress. There were no indications of osmotic adjustment to
water stress or that elevated [CO2] enhanced osmotic
adjustment in loblolly pine.
A number of recent studies have also confirmed that the
effects of elevated [CO2] on πo and osmotic adjustment are
minimal. Elevated [CO2] did not affect πo of honey mesquite (Polley et al. 1996, 1999), a species that is known to
osmotically adjust both diurnally and seasonally (Nilsen
et al. 1983). Similarly, Picon-Cochard & Guehl (1999)
reported that although elevated [CO2] increased sucrose
328 S. D. Wullschleger et al.
concentration by 20% in Pinus pinaster Ait., there was no
effect of CO2 treatment on soluble carbohydrate concentrations during a drying cycle, leading these authors to conclude that osmotic adjustment was not enhanced under
elevated [CO2]. The effects of elevated [CO2] on leaf πo of
two poplar (Populus sp.) clones were limited when grown
under conditions of non-limiting water availability (Tognetti et al. 1999b). Elevated [CO2] increased πo of Erica
arborea under drought, whereas πo declined in Juniperus
communis (Tognetti et al. 2000a). The largest differences in
midday leaf πo for species at the two study sites, the CO2
spring and control site, occurred in July. At that time, the
midday πo of Erica arborea was 0·36 MPa higher at the CO2
spring than at the control site, whereas πo of Myrtus communis did not differ between sites and πo of Juniperus
communis was 0·24 MPa lower at the CO2 spring. Site
(treatment) differences were less and likely not significant
(although trending in the same direction) when measured
in May and September.
In summary, the effect of elevated [CO2] on πo and
osmotic adjustment of leaves and roots is minimal and
probably an indirect, secondary response reflecting soluble
carbohydrate responses to sink demand imposed by the
CO2 treatments and prevailing growth conditions. The
varied, albeit limited, species-specific responses of πo to
elevated [CO2] suggest that rising [CO2] should not be considered as strictly beneficial with respect to this variable.
The higher net assimilation rates commonly observed with
CO2 enrichment do not necessarily result in higher solute
concentrations, particularly if organic solute turnover is
high, as in rapidly growing seedlings. It may take several
years of exposure to elevated [CO2] before soluble carbohydrate concentrations accumulate to appreciable levels in
specific tissues. We cannot assume that short-term increases
in growth can be sustained in the long term, as changing
sink demand may alter carbohydrate storage. Assessment
of osmotic potential, osmotic adjustment and/or solute
accumulation needs to include both foliage and roots given
their respective roles in water loss and acquisition. Errant
conclusions may result if only the osmotic response of
leaves to elevated [CO2] is characterized.
One factor that currently hinders our analysis is that
cause and effect relationships are only rarely established
between growth, gas exchange, anatomy and plant water
relations in the many CO2 enrichment studies conducted to
date. Instead, there is heavy reliance on inference. For
example, many investigators point to the observation that
elevated [CO2] often increases R/S ratio or fine-root proliferation, and then conclude that these effects must be beneficial to plants under water-limited conditions. Our
intuition supports this conclusion, but actual data fall short,
unfortunately, in supporting such causal associations. The
same concern can be raised in terms of the presumed benefits associated with CO2-induced effects on stomatal conductance, transpiration, WUE and leaf water potential. It is
rarely shown that these leaf-level impacts of elevated [CO2]
have implications to either the carbon or water balance of
leaves, whole plants or ecosystems. Grasslands and some
herbaceous crops apparently represent exceptions to this
rule.
We conclude that studies addressing the water relations
of plants exposed to elevated [CO2] and, in turn, the importance of observed responses to plants in water-limited environments, would benefit from a conceptual framework with
which to guide research, identify the need for new measurements and to evaluate the relationships among multiple
processes that ultimately contribute to plant growth and
development. We suggest that the hydraulic principles that
govern water transport provide such a framework, one that
allows integration of leaf-level processes including stomatal
conductance and water potential with the hydraulic architecture and transport efficiency of plants. Viewed from this
perspective, water uptake is controlled by soil and root
hydraulic properties, the transport characteristics of stems
including xylem anatomy and sapwood area, soil and leaf
water potential and stomatal conductance (Sperry 2000).
However, rather than being independent measures of
response, they are interrelated and collectively provide
insights into how elevated [CO2] and drought, through
effects on water relations, might potentially impact plant
growth and development in water-limited environments.
ACKNOWLEDGMENTS
CONCLUSIONS
The effects of elevated [CO2] on growth, gas exchange and
morphology and, in turn, the influence of these processes
on plant water relations are understandably critical issues
in predicting the productivity of plants and ecosystems in
water-limited environments. Predicting the response of terrestrial ecosystems to the interactive effects of elevated
[CO2] and drought will require that we understand processes that operate across a range of scales, including plants,
leaves, cells and molecules (Saxe et al. 1998). However, as
we have shown in this paper, at many (if not all) scales, the
implications of elevated [CO2] for WUE, water use and
whole-plant water relations become difficult to quantify
and interpret.
Manuscript reviews and comments for improvement were
kindly provided by C.A. Gunderson and A.M. Silletti.
Funding provided by the Office of Biological and
Environmental Research, US Department of Energy. Oak
Ridge National Laboratory is managed by UT-Battelle,
LLC, for the US Department of Energy under contract No.
DE-AC05–00OR22725.
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Received 16 March 2001; received in revised form 17 August 2001;
accepted for publication 17 August 2001