Journal of Arid Environments (2000) 45: 119}137

doi:10.1006/jare.2000.0638, available online at http://www.idealibrary.com on

Growth, photosynthesis and water-use efficiency of two

C4 Sahelian grasses subjected to water deficits

Joa o P. Maroco*, Joa o S. Pereira & M. Manuela Chaves

Instituto Superior de Agronomia, Tapada da Ajuda, 1399 Lisboa Codex,
Portugal

(Received 27 January 1999, accepted 29 February 2000)

Growth, photosynthesis and water use efficiency of two Sahel dominant

C grasses: Schoenefeldia gracilis Kunth and Dactyloctenium aegyptium (L) P.

Beauv were studied under well-watered and drought conditions. D. aegyptium
had a faster rate of development than S. gracilis and responded to water-deficits
by decreasing leaf area in the earlier stages of development. However, under
water-stress the overall reduction of leaf area suffered by S. gracilis was
greater than in D. aegyptium. The decrease in net photosynthesis observed
under water-deficits resulted mainly from stomatal closure. Analysis of correla-
tion between long-term water-use efficiency and several physiological,
structural and growth characteristics shows that long-term water-use effi-
ciency in D. aegyptium was positively correlated with relative growth rates. The
reduction in growth resulting from water-deficits was compensated by an in-
crease in the short-term water-use efficiency associated with stomatal clos-
ure. In S. gracilis, the long-term water-use efficiency under moderate water-
deficits increased but was not positively correlated with relative growth rate; it
was associated with a high allocation to non-photosynthetic (support and vascu-
lar) tissues. The possible implications of this behaviour for the different
‘strategies’ for plant survival in the arid climate of the Sahel are discussed.

 2000 Academic Press

Keywords: Dactyloctenium aegyptium (L.) P. Beauv; Schoenefeldia gracilis

Kunth; drought tolerance; drought avoidance; water-stress; water-use effi-
ciency; Sahel

Introduction

The Sahel region of Africa, located between 12 and 203 N in latitude is characterized by
a low rainfall (mean annual precipitation between 200 and 600 mm) and a long dry
season, which may be as long as 10 months in the north and 8 months in the south.
However, the most dramatic feature of the climate of this region is the variability in
rainfall between years (Grouzis, 1988; Wickens, 1997).
The seasonality of rainfall determines the phenology of native grasses. Grouzis (1992)
defined three phases in the development of the grassland cover: the establishment phase,
between April and June, requiring soil moisture reserves of about 10}20 mm; the fast
growing phase, between June and September, which corresponds to the rainy season;

*Corresponding author: Departamento de Engenharia Florestal, Instituto Superior de Agronomia, Tapada da

Ajuda, 1399 Lisboa Codex, Portugal.

0140-1963/00/060119#19 $35.00/0  2000 Academic Press

120 J. P. MAROCO ET AL.

and the third phase, the dry season from September through October, during which
shoots senesce and seed maturation and dissemination occurs. In most cases, the plants
cope with the irregularity of rainfall because they build up a relatively large stock of
hard seeds in the soil (Grouzis, 1992). These will germinate only after precipita-
tion is enough to guarantee adequate soil moisture for the first phase of canopy
development (Maroco, 1995). The earlier part of the growing season occurs when
air temperature is highest (May}June) and when temperature is above 203C.
Such environmental conditions would be favourable to a C type of photosynthetic

metabolism in grasses. However, the irregularity of rainfall often results in limitations to
soil water availability that will affect plant growth and survival and may change the
length of the growing season.
Growth is generally more sensitive to water-deficits than gas exchange, and reductions
in growth (mainly foliage) may occur at moderate soil water-deficits, even if plant
relative water content does not change significantly (Passioura, 1988; Kuang et al., 1990;
Gowing et al., 1990; Pereira & Chaves, 1993; Keya, 1998). However, the growth of
roots is usually less sensitive to water-deficits than that of the shoots (Sharp, 1990).
Therefore, acclimation to soil water-deficits, involving differential growth responses
in roots and shoots and increased stomatal closure, may reduce the ratio of transpiration
to water uptake from the soil, temporarily improving plant water content, delaying the
onset of the dehydration phase and therefore increasing survival (Pereira & Chaves,
1993; Maroco, 1995). In grasses, plant development and reproduction may also be
accelerated, either as a result of water-stress per se or because of higher air temperatures
that normally accompany the shortage of precipitation.
At the leaf level, stomata closure in response to moderate water-stress is the main
factor responsible for the differences in gas exchange between stressed and non-
stressed plants (Chaves, 1991; Cornic, 1994). Stomatal closure also results in a more
efficient loss of water per carbon assimilated (Farquhar et al., 1988; Davies &
Pereira, 1992; Jones, 1992). Additionally, non-stomatal effects on photosynthesis
may be responsible for inter- and intra- genotype differences in leaf water-use
efficiency (net CO assimilation per H O transpired, water-use efficiency, WUE),
 
namely between different C types (Fisher & Turner, 1978; Jones, 1992).

Long-term water-use efficiency (dry-weight accumulated per unit of transpired
water at the end of the season, WUELT) can be considered an important component of
drought tolerance (Martin et al., 1989; Edhaie & Waines, 1993; Udayakumar et al.,
1998) and improving WUELT has been a long-standing goal of plant breeders ( Johnson
& Basset, 1991; Udayakumar et al., 1998). It is important to identify the factors
underlying variations in the WUELT since they can be either positively or negatively
correlated with productivity, depending on the main processes determining changes in
WUE (see also Udayakumar et al., 1998). Variation in WUELT will have different
consequences on productivity, whether drought adaptation results from avoidance or
tolerance to water shortage. For example, a high WUELT may be detrimental in strict
drought avoiders if it results from stomatal closure, because these plants normally
complete their cycle with abundant water. On the other hand, if a greater WUELT results
from a higher photosynthetic capacity, the opposite may be true, because these plants
will have a greater production for a given amount of water transpired, as is the case for
C plants relative to C plants (Davies & Pereira, 1992; Henderson et al., 1994).
 
Although the differences in WUELT between C and C plants are well known,
 
there is also experimental evidence for intra- and inter-species variability within each
group (Martin & Ruiz-Torres 1992; Monjayad & Planchon, 1994; Kramer & Boyer,
1995). C plants have generally high intrinsic WUE (net assimilation rate over stomatal

conductance, A/g ) and instantaneous WUE (net assimilation rate over transpiration,
Q
A/E) due to lower stomatal conductance and higher photosynthetic capacity. This
behaviour has strong implications for the strategies that this type of plant follows to use
water efficiently and is believed to be responsible for adaptation and evolution of
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 121

C plants in arid climates, and for the geographic distribution of the three different

C types (Edwards et al., 1985; Henderson et al., 1994). For example, Henderson et al.

(1994) observed that whereas phosphoenolpyruvate carboxykinase (PEP-CK) type
species, such as D. aegyptium (Lin et al., 1993) have a relative occurrence in regional
floras independent of the rainfall pattern, distribution of Nicotinamide-adenine dinuc-
leotide Malic enzyme (NAD-ME) type species (such as S. gracilis, unpublished observa-
tions) is strongly and negatively correlated with the median annual rainfall.
The aim of this paper was to study the effects of water-deficits on growth and to
identify physiological, structural and growth ‘strategies’ that may explain differ-
ences in adaptation, productivity and WUELT of two dominant C grasses (S. gracilis

and D. aegyptium) of a naturally arid ecosystem, the Sahelian rangelands.

Material and methods

Plant material and growth conditions

Seeds of Schoenefeldia gracilis Kunth and Dactyloctenium aegyptium (L.) P. Beauv were
collected at Dahra-Djollof in the Senegalese Sahel (15323N, 15330W). Additional
seeds of D. aegyptium were obtained from Kew Royal Botanical Gardens (West Sussex,
UK). Uncoated seeds of S. gracilis and scarified seeds of D. aegyptium were germinated
on moistened filter paper or 1% agar in a germination chamber (Aralab, Lisbon)
with 40 lmol m\ s\ PAR from fluorescent bulbs, 12h light/12h dark photoperiod and
313C day/213C night temperatures. Germinated seeds were transplanted to 7)4-litre pots
filled with a mixture of peat and sand (1 : 1) fertilized with one kg of a commercial fertilizer
(15 : 11 : 13 : 2; N : P : K : Mg) per m of soil and a micronutrient solution (commercial
fertilizer JLV, Lisbon). Plants were grown for 120 days in a greenhouse in Lisbon
(38342N, 9311W) with temperatures varying between 20 and 353C, relative humidity
between 15 and 85% and average daily PPFD of 502$47)8 lmol m\ s\ during the
growth period. Up to the 36 day after emergence (DAE) all plants were kept well-
watered (soil near field capacity). Afterwards, the pots were subjected to two watering
regimes: high water (HW), plants watered every 2}3 days with 100% of transpired water
in the same period, calculated by weighing of the pots; low water (LW), plants watered
every 2}3 days with 50% of transpired water. Water was applied from 10 to 30 cm below
the surface of the pots through a perforated tube. Evaporation losses were prevented by
covering the pot surface with a thick layer (2 cm) of polyethylene spheres.

Growth analysis and gas exchange measurements

Four harvests for biomass determination were done at 30-day intervals (i.e. at 30, 60, 90
and 120 days after emergence, DAE). At each sampling time, four plants per species and
per treatment were collected and separated into components (leaves, stems, roots). The
dry mass (DM) of each plant component was obtained after 48 h in an oven at 803C.
Leaf area (S) was measured with a Li-3000 portable area meter (Li-Cor Inc., Lincoln,
USA). The relative growth rate (RGR), the net assimilation rate (NAR), the leaf area
duration (LAD), leaf weight ratio (LWR) and specific leaf area (SLA) were calculated
as described in Radford (1967) and Beadle (1993).
Gas exchange measurements were performed with a portable photosynthesis open
system CI-301PS (CID Inc., Vancouver, USA) under natural daily growing conditions
using standard gas-exchange formulae (von Caemmerer and Farquhar, 1982). Photo-
synthetic capacity (A ) i.e. oxygen evolution at CO and light saturation, was deter-
 
mined in a leaf-disc oxygen electrode (Hansatech Ltd., Kings Lynn, UK), at 303C with
a PPFD of 1200 lmol m\ s\ and saturating CO concentration (10% CO provided
 
122 J. P. MAROCO ET AL.

by mixing air and CO ), immediately after detaching the leaves. The chlorophyll a fluores-

cence was measured using a portable pulse amplitude modulation fluorometer (PAM
2000, Heinz Walz, Effeltrich, Germany). The quantum yield of non-cyclic electron
transport ('e) of leaves in light adapted state was calculated as in Genty et al. (1989).

Water potential and WUE measurements

*2
Plant water status in HW and in LW plants was followed by measuring leaf water
potential at predawn ((pd) with an Scholander type pressure chamber (PMS instru-
ments Co., Corvallis, USA). In LW plants the (pd was always measured one day after
watering. Transpiration (E) was determined gravimetrically on each plant. Water-use
efficiency was calculated both as the ratio of net photosynthetic rate and stomatal
conductance, the intrinsic WUE (WUEi ), and as the ratio of the biomass produced and
the water transpired during the same period, the long-term WUE (WUELT).

Chlorophyll determination, C discrimination and histo-anatomical observations

Chlorophylls were determined accordingly to Arnon (1949). C discrimination was

determined as described in OsoH rio et al. (1998). Plant tissues for histo-anatomical
observations were prepared as described by Dougherty (1981). Ten-lm slices were
stained and observed under a light-microscope (Dialuz 20 EB, Leitz, Germany). Images
were collected with a video-camera (VarioScan V1.6, Leitz, Wetzlar, Germany) and
analysed using the ASM 68K software (Leitz, Wetzlar, Germany).

Statistical analysis

Correlations between the WUELT and the physiological and growth parameters were
analysed by standard methods of Pearson-Correlation analysis. The significance of the
differences between the two watering treatments and the two species was analysed
by means of a standard two-way ANOVA with significance level p"0)05. Data points
are the averages of four replicates and differences between the means were analysed
by Tukey’s Least Significant Differences.

Results

Soil water availability significantly affected the dry-matter accumulation, leaf area,
transpiration and tpd of D. aegyptium (d13C"!15)10$0)03) and S. gracilis (d13C"
!15)88$0)34) (p(0)01, Fig. 1) which both have a C type of photosynthesis judging

from 13C discrimination analysis and anatomical observations (not shown). In
D. aegyptium, biomass was approximately four-fold lower, while leaf area was two-fold
lower in LW as compared to HW plants at the end of the experiment. In S. gracilis, LW
plants had a reduction of approximately three-fold in biomass and of approximately
four-fold in leaf area when compared to HW plants (Fig. 1(a, b)). The accumulated
transpiration was approximately four-fold lower in the LW treatment relative to the HW
treatment in both D. aegyptium and S. gracilis (Fig. 1(c)) and D. aegyptium had lower
tpd values (!2)5 MPa) than S. gracilis (!1)5 MPa) at the end of the experiment (Fig.
1(d)).
The leaf area duration (LAD) for the period of the experiment (which in S. gracilis
HW plants did not correspond to the end of the life cycle) decreased in LW plants, by
1)6 times in D. aegyptium and by 3)2 times in S. gracilis, relative to HW plants (Fig. 2).
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 123

Figure 1. Changes with time in: (a) dry matter production, DM; (b) leaf area, S, (c) transpira-
tion, E; and (d) predawn leaf water potential, (pd (mean$2S.E.) of D. aegyptium ( , HW;
, LW) and S. gracilis ( , HW; , LW) plants. See text for details on treatments.

Figure 3 illustrates the changes in growth rates of the two species versus time and water
availability. D. aegyptium developed faster and was particularly efficient in ac-
cumulating biomass in the early stages of the life cycle when the relative growth rate
(RGRB) was significantly higher (p(0)01) than in S. gracilis (Fig. 3(a)). After 30 DAE,
water-stress did not produce statistically significant differences for the RGRB of
both species when these rates were averaged over a 30-day period. There were no
significant differences in leaf area relative growth rate (RGR ) for S. gracilis under
1
both watering regimes. However, D. aegyptium plants had significantly lower (p(0)01)
124 J. P. MAROCO ET AL.

Figure 2. Leaf area duration (mean$2S.E.) in D. aegyptium and S. gracilis for the whole study
period (i.e. up to 120 DAE). , HW; , LW.

RGRS under water-stress. In contrast, drought-stressed plants had higher NAR than
well-watered plants at 60 and 90 DAE, but not at 120 DAE (Fig. 3(b)). For S. gracilis,
a significantly higher NAR under water-stress was achieved after 60 DAE (Fig. 3(c)).
The SLA decreased along the life cycle of both species and drought-stressed plants
had lower SLA than well-watered plants, although the differences were only
statistically significant for 30 and 60 DAE (Fig. 4(a)). The LAR can be quantified as the
product SLA;LWR. Figure 4(b) shows that most of the decrease in LAR for both
species and water regimes, in the first period (30}60 DAE) resulted from changes in
SLA—a strong decline in D. aegyptium and a slight decrease in S. gracilis. The variation
in LWR with time (Fig. 4(c)) was statistically significant (p(0)05) in D. aegyptium but
not in S. gracilis (p'0)05). Another important difference between the two species
was the higher proportion of vascular and support tissues in the leaves of S. gracilis as
compared with D. aegyptium (Table 1). S. gracilis had a significantly higher proportion
of vascular and support tissues than D. aegyptium. However, while in S. gracilis these
proportions were not affected by water-stress (p'0)1), in D. aegyptium water-
stress increased the proportion of vascular and support tissues, although not at a statist-
ically significant level (Fig. 4(a, b) and Table 1.). The reduction in plant leaf area and in
SLA, followed by an increase in structural and vascular tissues in leaves explains why, in
contrast with LAR, the leaf weight ratio (LWR) was not significantly affected by
soil water-deficits (with the exception of the period from 90 to 120 DAE,
Fig. 4(c)).
In spite of the differences observed in dry-matter accumulation and in NAR
between the two species and between the two water regimes, no significant differ-
ences were observed throughout the growing cycle in maximal gas exchange rates
(measured during the day under growing conditions, Fig. 5). However, the maximum
occurred early in the morning for LW plants, whereas in HW plants maximal values
were attained at midday, as shown for day 60 after emergence (Fig. 6). Similarly, no
statistically significant differences were found in the integral of daily photosynthetic
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 125

Figure 3. (a) Relative growth rate in biomass; (b) relative growth rate in leaf area, RGRs; and (c)
net assimilation rate, NAR (mean$2S.E.) of D. aegyptium ( , HW; , LW) and S. gracilis ( ,
HW; , LW) plants.

water-use efficiency between watering regimes for the same species (Fig. 7), which
resulted from the coupling of stomatal control of transpiration with photosynthetic
capacity. The absence of significant difference in the daily maximal net photosyn-
thetic rate (A dmax) between HW and LW plants of both species is compatible with the
maintenance of the photosynthetic capacity (Amax, measured at saturating CO ) in the

mature leaves of LW plants (Table 2). On the other hand, photosynthetic capacity
decreased significantly (p(0)01) throughout the growing season in both species,
accompanying the general decline in SLA and in total chlorophylls (Table 2). Drought-
stressed plants of both species had a higher chlorophyll content than well-watered plants
at 120 DAE (p(0)05).
At the photochemical level, D. aegyptium had significantly higher maximum quantum
yield of PSII (Fv/Fm) than S. gracilis (p(0)001). Water-stress did not significantly
affect the Fv/Fm ratio of either species (Table 3). However, when the maximum
quantum yield of CO fixation under limiting light and saturating CO (5%) conditions
 
was measured, the effect of water-stress was statistically significant (p(0)05) for
D. aegyptium, but not for S. gracilis (Table 3).
126 J. P. MAROCO ET AL.

Figure 4. (a) Specific leaf area; (b) leaf area ratio, LAR; and (c) leaf weight ratio, LWR
(mean$2S.E.) of D. aegyptium ( , HW; , LW) and S. gracilis ( , HW; , LW) plants.

Despite the differences in growth rates, leaf area and plant structure, by the end
of the experimental period (120 DAE) both species had similar WUELT (Fig. 8).
D. aegyptium achieved maximum WUELT at 60 DAE, and then WUELT decreased as
a result of preferential biomass allocation towards reproductive organs (data not shown).
For this species, the differences in WUELT for both water regimes were only
significant at 90 DAE (p(0)01). In contrast, WUELT for S. gracilis increased continu-
ously up to 120 DAE and was significantly higher in LW plants (p(0)05).
Pearson-correlation analysis between WUELT and several physiological, structural
and growth indicators are shown in Figure 9. For D. aegyptium the WUELT was
significantly correlated with RGR of both biomass and leaf area. In HW plants of this
species, WUELT was also positively correlated with leaf area growth, as suggested by the
significant correlations obtained between WUELT and LWR, and LAR and RGRS. For
LW plants, however, in addition to RGRB, the best correlation of WUELT was with
NAR. Predawn leaf water potentials, maximum net photosynthesis and stomatal con-
ductance did not correlate significantly with WUELT for both LW and HW plants. The
same was observed with the correlation between WUELT and the daily maximum
photosynthetic water-use efficiency (WUE dfmax) in HW plants, however in LW
plants the WUELT was negatively associated with WUE dfmax.
 Table 1. Evolution of the relative area (%) of the leaf vascular bundles, parenchyma and colenchyma in D. aegyptium and S. gracilis

WATER-USE EFFICIENCY OF SAHELIAN SPECIES

DAE 60 90 120

HW LW HW LW HW LW

D. aegyptium
Vascular bundles 5)9(0)2) 7)0(1)5) 3)7(0)4) 5)8(1)3) 3)7(0)3) 4)4(0)9)
Parenchyma 92)1(0)4) 90)11(1)8) 95)1(0)6) 92)7(1)3) 95)1(0)4) 93)6(1)2)
Collenchyma 1)9(0)3) 2)8(0)4) 1)1(0)2) 1)5(0)5) 1)1(0)2) 2)0(0)3)
S. gracilis
Vascular bundles 12)7(0)7)
12)2(0)7)
12)1(0)6)
11)8(1)6)

Parenchyma 72)2(2)0) 75)2(1)1) 72)8(2)2) 72)1(3)4)
Collenchyma 15)2(1)9) 12)6(1)0) 15)1(2)6) 16)0(3)3)

Data shown is the averages of four replicates with the standard error of the mean between parenthesis. Different letter suffixes indicate statistically significant
differences between species and water-stress treatments at p"0)05.

127
128 J. P. MAROCO ET AL.

Figure 5. (a) Daily maximum net photosynthesis, A; (b) stomatal conductance g ; and (c)
Q
intrinsic water-use efficiency, WUEi (mean$2S.E.) of D. aegyptium ( , HW; , LW) and
S. gracilis ( , HW; , LW) plants.

In S. gracilis, the WUELT was negatively associated with SLA, LWR and LAR
(Fig. 9). The apparent lack of effect of water-stress over the associations between
leaf structural indicators and WUELT suggests that this association may be under tight
genetic control, rather than enhanced by the environment (water-stress) as observed in
D. aegyptium. NAR was positively associated with WUELT for both HW and LW plants.
For LW plants of this species, WUELT was also negatively associated tpd , but no
significant correlation was found for maximum gas-exchange rates and relative growth
efficiencies.

Discussion

Soil water-deficits affected growth characteristics and biomass accumulation of

both D. aegyptium and S. gracilis (Fig. 1). Generally, when water is not restrict-
ing growth, herbaceous plants invest a considerable fraction of photoassimilates in
the expansion of photosynthetic tissues, maximizing light interception and, as a
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 129

Figure 6. (a) Daily courses of stomatal conductance; (b) net photosynthesis; (c) intrinsic water-
use efficiency; (d) leaf temperature; (e) leaf to air vapour pressure deficit measured in Lisbon
(f ) photosynthetic photon flux density ( , HW; , LW) and S. gracilis ( , HW; , LW) at 60
DAE (mean$2.S.E.).

consequence, growth (Fisher & Turner, 1978; Dale, 1988). However, under water-
stress a different strategy imposes a different pattern of allocation of assimi-
lates, resulting in the decrease of leaves relative to other organs, or the alteration of the
relative amounts of photosynthetic and non-photosynthetic tissues (Fisher & Turner,
130 J. P. MAROCO ET AL.

Figure 7. Daily integrals of the ratio A/E (mean$2S.E.) for D. aegyptium ( , HW; , LW)
and S. gracilis ( , HW; , LW).

1978). In spite of approximately four- and three-fold reductions in final biomass (for D.
aegyptium and S. gracilis, respectively) in drought-stressed relative to well-watered
plants, the relative growth rates, measured over a 30-day period, were not significantly
reduced by soil water-deficits in either species (Fig. 3). This does not mean we must
discard the hypothesis that shorter-term changes in the RGR may have occurred.
However, these hypothetical differences may have been lost when the rates were
averaged over a 30-day period. There was a substantial reduction in leaf area growth
caused by water-stress in both species as expressed by the decrease in the leaf area
duration (Fig. 2). Fast growing species such as D. aegyptium, are more sensitive to low
soil water availability and delay the onset of plant dehydration by an early reduction in
leaf area (cf. Fig. 1(d) for the seasonal course of W ). However, the overall reduction in

leaf area estimated by the changes in LAD (Fig. 2) was greater in S. gracilis. The rapid
growth of D. aegyptium in the beginning of the life cycle was coincident with a rapid
display of foliage area (high LAR) coupled with a higher photosynthetic capacity, which
was more related with a high SLA than with a large ‘investment’ of biomass in leaf tissue
(Figs 2 and 3). This is a component of the ‘fast growth syndrome’ (Pereira, 1993) of
D. aegyptium, in comparison with S. gracilis. Another major difference between
S. gracilis and D. aegyptium was related to the higher proportion of vascular and support
tissues in leaves in the former both in well-watered plants and in water-stressed plants
(Table 1). Plant development enhanced the proportion of leaf support tissues at the
expense of metabolically active cells (explaining the decline in SLA), paralleled by
a decrease in leaf chlorophyll, photosynthetic capacity and stomatal conductance
(Tables 2 and 3). Increased efficiency of sieve transport, as a result of an increase in
vascular vs. mesophyll tissues, is common in a large number of xerophytic plants
(Nobel, 1990, 1991; Bolhàr-Nordekampf & Draxler, 1993).
The higher photosynthetic capacity (and
) of D. aegyptium as compared with

S. gracilis led to a marginal increase in the net photosynthetic rate under growing
conditions. This suggests that stomata were the main limitation to photosynthesis under
the growth conditions prevailing during the experiment. Under water-deficits, the main
difference relative to well-watered conditions was that maximum photosynthesis
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES
Table 2. Evolution of the total chlorophylls (gm\2) and maximum photosynthetic capacity (kmol O2m\2s\1) in D. aegyptium and S. gracilis.

D. aegyptium S. Gracilis
Chlorophyll Amax Chlorophyll Amax

DAE HW LW HW LW HW LW HW LW

30 0)48(0)02)  0)47(0)02)  60)8(6)0) 60)8(6)0) 0)52(0)08)
0)52(0)08) 45)2(6)3)
45)2(6)3)

60 0)43(0)03)  0)42(0)06)  38)5(2)3)
30)5(1)9)
 0)34(0)08)
0)29(0)05)
24)9(6)4) 27)1(1)4)

90 0)35(0)04)  0)44(0)03)  28)8(3)0)
 16)5(3)2) 0)19(0)02)
0)28(0)05)
 20)2(2)0) 24)3(1)9)
120 0)13(0)01)
0)42(0)01)  18)2(3)2) 11)7(3)7) 0)22(0)03)
 0)42(0)06)  8)5(3)2) 12)3(1)2)

Data shown is the averages of four replicates with the standard error of the mean between parenthesis. Different letter suffixes indicate statistically significant
differences between species and water stress treatments at p"0)05.

131
 132
Table 3. Evolution of the maximum quantum yield of PSII (Fv/Fm) and maximum quantum yield of CO fixation (
CO ) in D. aegyptium
and S. gracilis.  

D. aegyptium S. Gracilis

J. P. MAROCO ET AL.
Fv/Fm
CO Fv/Fm
CO
 

DAE HW LW HW LW HW LW HW LW

30 0)80(0)01)  0)80(0)01)  0)067(0)004) 0)067(0)004) 0)66(0)03)
 0)66(0)03)
0)037(0)005)
 0)037(0)005)


60 0)79(0)01) 0)78(0)01)
0)051(0)009)
0)029(0)006) 0)62(0)03)
0)58(0)01)
0)021(0)004) 0)022(0)002)
90 0)73(0)02)
 0)81(0)02) 0)040(0)004) 0)018(0)004) 0)67(0)04)
0)72(0)01)
 0)018(0)003) 0)014(0)002)
120 0)75(0)04)
 0)74(0)02)
0)039(0)003) 0)018(0)002) 0)76(0)01)
0)66(0)03)
 0)029(0)002) 0)035(0)003)


Data shown is the averages of four replicates with the standard error of the mean between parenthesis. Different letter suffixes indicate statistically significant
differences between species and water stress treatments at p"0)05.
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 133

Figure 8. Long-term water-use efficiency (mean$2S.E.) D. aegyptium ( , HW; , LW)

and S. gracilis ( , HW; , LW).

and stomatal conductance occurred earlier in the day in LW than in HW plants. This is
compatible with the lack of effects of moderate water-stress on photosynthetic
capacity (measured at saturating light and CO ) and at the photochemical level as

observed in C species (Genty et al., 1987; Chaves, 1991; Cornic, 1994) as well as in

other C species (Cornic & Ghashghaie, 1991; Havaux, 1992; Lal & Edwards, 1996).

The main effect of moderate soil water-deficits on photosynthesis was, therefore,
the stomatal closure earlier in the day, leading to a decrease in net carbon assimilation
per unit leaf area and per day. However, when the integral for the daily WUE is
calculated, not statistically significant differences were found between well-watered
and water-stressed plants (Fig. 7). These results suggest that an efficient stomatal
control over transpiration, coupled with the maintenance of the photosynthetic capacity
(Fig. 6) allows these species to control their daily water-use efficiency. Therefore,
reduction of plant growth under water-stress conditions can be explained by the
reduction in leaf expansion, since both maximum photosynthetic capacity and max-
imum stomatal conductance were not significantly affected by water-stress. The
reduction in biomass observed under drought-stress, with maintenance of photosyn-
thetic capacity, may be the reason why drought-stressed plants had higher NAR (Fig. 3).
Preferential maintenance of photosynthetic machinery, vascular and support tissues,
associated with a reduction in biomass at early stages of drought may increase the
efficiency of pre-existing biomass for de novo growth. Whenever stomata can fully
open (e.g. during intercalary rains), the maintenance of photosynthetic capacity will be
beneficial, as the plant may profit, in terms of CO uptake, from a temporary and

random water availability, as happens frequently in the Sahel.
The absence of a significant positive correlation between WUEdfmax and WUELT
reflects the difference in time scale of both processes (from seconds to months) and
non-accounted energy expenses in growth and maintenance in the long-term water-use.
Although it can be expected that species with higher instantaneous WUE may have
higher WUELT (Fisher & Turner, 1978; Edwards et al., 1985), the evolution of both
efficiencies may not be correlated, due to differences in the partition of the
photoassimilates for growth, maintenance and reproduction at different plant ages.
The lack of statistically significant differences in the instantaneous WUE between
the two different watering regimes seems to be characteristic of C species, as

134 J. P. MAROCO ET AL.

Figure 9. Pearson correlations between long-term water-use efficiency and photosynthetic,

structural and growth and assimmilation efficiency variables D. aegyptium ( , HW; , LW)
and S. gracilis ( , HW; , LW). Probability as follows: ns"p'0)05; *0)05(p(0)01;
**0)01(p(0)001; ***(p(0)001.

observed also by Kirkham et al. (1991) and Gifford & Morrison (1985). However,
the differences in WUELT between water-stressed and non-stressed plants seem to
be dependent on the phenological stage. While the differences are only statistically
significant at 60 DAE for D. aegyptium, in S. gracilis the higher WUELT of LW plants is
never statistically significant, in accordance with other reports on long-term WUE of C

plants (Fisher & Turner, 1978; Turner, 1986; Jones, 1992). This behaviour in WUELT
seems to be characteristic of a number of C4 species, while others show higher WUE
under water-stress (e.g. Gifford & Morison, 1985; Johnson & Basset, 1991).
The WUELT of D. aegyptium was positively correlated with RGR in agreement with
observations made in other species (e.g. Hubick et al., 1986). However, for S. gracilis
WUELT had the strongest positive association with NAR and a negative association with
SLA. These results suggest that the species in this study have different strategies to
cope with, and survive drought-stress. Whereas D. aegyptium maximizes its growth
efficiency for the available water resources, with acceleration of its life cycle, the
S. gracilis strategy is oriented towards the reduction of water losses and dehydration.
Although, greenhouse conditions are generally less harsh than natural conditions,
namely due to smaller climatic (temperature, light, LAVPD, etc.) variations, the ‘behav-
iour’ observed in response to drought inside a greenhouse may reflect a species ‘strategy’
to cope with their natural environment. D. aegyptium and S. gracilis are both C species,

but the main factors determining long-term WUE may be different, as suggested by
Pearson-correlations analysis. D. aegyptium was particularly efficient in using water
 WATER-USE EFFICIENCY OF SAHELIAN SPECIES 135

in early stages of the life cycle when higher growth rates (of biomass and leaf area)
occurred. This behaviour suggests that this species is mainly a ‘drought avoider’ i.e. it
completes its life cycle before the onset of drought, using the maximum of available
resources, namely water and light. Long-term WUE is determined by the efficiency
in using those resources for growth. In S. gracilis, however, WUELT under moderate
water-deficits was not positively correlated with relative growth rates and was mainly
associated with an investment in non-photosynthetic tissues (negatively correlated with
LWR). This suggests that this species has a ‘strategy’ of drought tolerance, based on
preferential allocation towards vascular and support tissue as well as roots (data not
shown), thereby postponing dehydration when soil moisture is being depleted. Long-
term WUE in this species is mainly associated with the conservative use of available
water resources. Since S. gracilis has a slower growth and a longer growing season than
D. aegyptium, this strategy may be more advantageous for survival under the sparse and
irregular rainfall pattern of the Sahel.

Thanks to T. Nolan and J. Connoly, and Agronomist C. Shall for logistic support in seed
collecting. The EU Project, Contract No. TS3-CT93-0202, financed this work. Financial support
to one of us ( JPM) was provided by a scholarship from the ‘Junta Nacional de Investigaia o
Cientifica e TecnoloH gica’ (contract no. BM/3112/92-IE), Lisbon, Portugal. We also would like to
thank P. Jackson for the critical review of the manuscript as well as two anonymous reviewers for
their comments.

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