173 D.W. Lucero et al. European Journal of Agronomy 11 1999 167–177
action, but was due more to a decrease in shoot Increasing soil water deficit had a much greater
effect on secondary LAR than on primary LAR growth than to an increase in root growth, as soil
volume in this experiment was restricted. [Fig. 2b]. White clover subjected to no soil water
deficit and grown in no interaction had twice as high a secondary LAR as the other two interaction
3.5. Stolon growth and relative growth rate treatments. Total LAR was highest for white clover
grown in no interaction at no soil water deficit, Average stolon and stolon internodal length
decreased as soil water deficit increased [Fig. 1a almost twice as much as the other interaction
treatments and soil water deficits [Fig. 2c]. At and b]. At no and moderate soil water deficit,
average stolon and stolon internodal length was moderate soil water deficit a similar total LAR
was observed for each interaction treatment; how- highest in white clover grown in shoot+root inter-
action, followed by plants grown in no interaction ever, the total LAR of white clover grown in
shoot+root interaction was the most severely and then by plants grown in shoot interaction. At
severe soil water deficit, white clover grown in reduced when soil water deficit was severe.
shoot+root interaction had shorter stolons than white clover grown in either no interaction or in
shoot interaction. For average stolon internodal
4. Discussion
length this same relationship was true for white clover grown at each soil water deficit level.
Van Loo 1992 observed that root growth of ryegrass plants grown individually was reduced
Stolon RGR decreased as soil water deficit increased [Fig. 1c]. The RGR of stolons was
more than shoot growth at similar soil water deficit levels to those used in this study. In our study,
substantially higher at no and moderate soil water deficit than at severe soil water deficit for white
increased soil water deficit decreased root DM yield for ryegrass grown in no interaction. Plant
clover grown in shoot+root interaction. Stolon RGR for white clover grown in shoot+root inter-
interaction shoot or shoot+root lessened the effects of reduced ryegrass root DM yield that was
action at moderate soil water deficit was as high as that observed for white clover grown in shoot
observed in ryegrass grown in no interaction. That white clover root DM yield was only slightly
interaction at no soil water deficit. At no and moderate soil water deficit, the order of white clover
affected by increased soil water deficit could be attributed to the smaller root system of white
stolon RGR was: shoot+root interactionno interactionshoot interaction; however, at severe
clover compared with grasses Thomas, 1984. In a restricted soil area, such as that used in this
soil water deficit this trend was: no interaction shoot interactionshoot+root interaction.
study, the degree to which white clover root sys- tems could have been reduced by soil water deficit
was thus less than for ryegrass. 3.6. Leaf appearance rate
Wilson 1988 reported that root competition had a greater effect than shoot competition in 70
Highest primary LAR was observed for white clover grown in no interaction at no soil water
of 47 cases found in the literature and concluded that root competition is usually more important
deficit [Fig. 2a]. White clover grown in no inter- action had higher primary LAR at each soil water
than shoot competition in determining competitive balance, the intensity of competition, and resource
deficit level than white clover grown in shoot interaction. The highest primary LAR observed at
use. Root DM yield of ryegrass was double that of white clover in this experiment Table 1. Jupp
moderate soil water deficit level was for white clover grown in shoot+root interaction. White
and Newman 1987 observed that water-stressed ryegrass plants had three to five times more lateral
clover grown in shoot+root interaction at moder- ate soil water deficit had as high a primary LAR
root initiation and growth than controls at severe soil water deficit. The ability of one plant to extract
as white clover grown in either no interaction or in shoot interaction at no soil water deficit.
soil water compared with another plant can be
174 D.W. Lucero et al. European Journal of Agronomy 11 1999 167–177
enhanced by greater root densities. In this study, shoot or shoot+root, offset the propensity of white
clover to flower under water stress Table 2. ryegrass grown in shoot+root interaction at severe
soil water deficit was more competitive for soil Generally, white clover spreads vegetatively by the
growth of stolons and, therefore, is continually water than white clover. Burch and Johns 1978
have also observed that white clover grown in establishing new, adventitious root systems from
stolon nodes. The long-term sustainability of white competition with Festuca had poorer control of
leaf transpiration, which resulted in low leaf water clover in mixed swards subjected to soil water
deficits could, however, still be compromised by potentials and increased leaf senescence. Grasses,
on the other hand, have better stomatal control the reduction in inflorescence caused by plant
interaction observed in this study. and higher leaf water potential, which increased
and prolonged grass growth in drought conditions The increased DM yield observed at no and
moderate soil water deficits for ryegrass grown in Johns and Lazenby, 1973; Thomas, 1984. This
may further explain why, in this study, reductions shoot+root interaction compared with shoot inter-
action with white clover could be attributed to in the shoot DM yield of white clover subjected
to severe soil water deficit were considerably increases in N availability through N fixed by
white clover, though this was not measured in greater than for ryegrass, and especially when the
two plants were grown in shoot+root interaction. our study. The transfer of N fixed atmospheri-
cally from white clover to companion grasses is Stolon growth and RGR and LAR of white
clover were markedly reduced by increased soil well documented and can amount to about
70 kg ha−1 per year Ledgard, 1991; this may water deficit Turner, 1991; Belaygue et al., 1996.
In our study, shoot+root interaction lessened the explain why ryegrass grown in shoot+root inter-
action with white clover produced more shoot DM reduction in stolon growth due to soil water deficit
that was observed for white clover grown in shoot than when grown in just shoot interaction with
white clover. Shamsun-Noor et al. 1989 studied interaction. Beinhart 1963 has shown that the
most marked effect of shading on white clover was the effects of drought on white clover and reported
that N fixation rates were maximum at soil water the reduction in the formation of stolons from
auxiliary buds. In this study, stolon length and deficits of between 60 and 70
, a level quite similar to that used in this study to define moderate soil
RGR were markedly reduced by shoot interaction compared with plants grown in no interaction,
water deficit. The optimization of N fixation by white clover at this level of soil water deficit has
yet at no and moderate soil water deficit levels stolon length, internodal length and RGR were
also been observed for white clover grown in sandy soil by Laperrie`re 1984 and Holter 1978 and
highest for plants grown in shoot+root interaction [Fig. 1a–c].
by Wahab and Zahran 1983 for red clover and alfalfa. In our experiment, the removal of soil
For white clover grown in no interaction or in shoot interaction, increased soil water deficit did
inorganic N by the roots of ryegrass grown in interaction with white clover would have led the
not change the percentage of stolon as part of shoot DM yield Table 2. However, increased soil
companion white clover plant to increase N fixa- tion in order to obtain sufficient N for growth.
water deficit did change leaf as a percentage of shoot DM yield in white clover plants grown in
Inorganic N can inhibit many phases of the N fixing process Postgate, 1982. However, Morris
no interaction or in shoot+root interaction. For plants grown in no interaction, flowers as a percen-
and Weaver 1987 have observed that N fertilizer rates did not significantly reduce the amount of N
tage of shoot DM doubled at each increase in soil water deficit — this increase was at the expense of
fixed by clover in clover and ryegrass mixtures due to grass removal of soil inorganic N.
leaf DM yield. It has been observed that soil water deficit can affect the balance between vegetative
Additionally, at no and moderate soil water deficit, the shoot DM yield of white clover grown
and reproductive growth in white clover plants Turner, 1991 and that long-term soil water deficit
in shoot+root interaction was higher than when grown in just shoot interaction Table 1. This
promotes the production of inflorescences Turner, 1993. In our study, plant interaction, whether
increased shoot DM yield was in the form of leaf,
175 D.W. Lucero et al. European Journal of Agronomy 11 1999 167–177
especially petiole. Also, white clover grown in soil water deficit Burch and Johns, 1978. Burch
shoot+root interaction at no and moderate soil and Johns 1978 have also shown that, owing to
water deficit had the highest percentage of shoot white clover poor stomatal control during a severe
growth in the form of leaf 69 and 68.5 and the
drought, leaf senescence is a mechanism used by lowest in the form of stolon 28 and 31
white clover to balance rate of transpiration rate Table 2. Though stolon, as a percentage of
and water uptake. In our experiment, white clover above-ground DM, was the lowest of all treat-
drought avoidance in response to severe soil water ments, it must be noted that stolon length, inter-
deficit can explain the low shoot DM yield nodal length and RGR were still the highest of all
Table 1 and more importantly the low leaf DM treatments [Fig. 1a–c]. As mentioned pre-
yield as a percentage of shoot DM yield observed viously, the moderate soil water deficit level used
for white clover grown in shoot+root interaction in this experiment has been shown to optimize
Table 3. The more efficient control of stomatal white
clover N
fixation Laperrie`re,
1984; closure and ability to reduce transpiration by leaf
Shamsun-Noor et al., 1989, which would have rolling in response to severe soil water deficit
favored white clover DM yield. Additionally, allowed ryegrass to prolong its growth period and
Tomm et al. 1994, in a short-term N-transfer furthered ryegrass competitiveness for limited soil
experiment, showed that N is transferred from water when grown in shoot+root interaction in
both the N-fixing legume to an associated non- our experiment.
legume and also from the non-legume to the Though no N fixation parameters were mea-
N-fixing legume. In this manner, where there was sured in our experiment, the reduction in shoot
shoot+root interaction in our experiment between DM yield observed for white clover grown in
ryegrass and white clover, increased N from white shoot+root interaction at severe soil water deficit
clover fixation that benefited ryegrass DM yield level might have been due to a reduction in atmo-
could also have benefited white clover growth. The spherically fixed N by white clover nodules. Wilson
question of
ryegrass shoot+root
interaction 1931 first reported that drought adversely
increasing the soil mineral uptake by white clover affected legume root nodules. Engin and Sprent
must also be asked. Whatever the reason, the 1973 attributed the initial effect of drought on
response of white clover grown in shoot+root interaction to produce more petiole leaf material
would have favored white clover photosynthetic
Table 3 Variance ratios for plant interaction PI , soil water deficit
activity by positioning a maximum amount of leaf
WD and plant interaction by soil water deficit PI×WD for
lamina to receive sunlight. A higher efficiency of
ryegrass and white clover plant part dry matter yield
white clover to intercept light has been observed in mixed swards Dennis and Woledge, 1985;
Dry matter F association
F water F interaction
Woledge, 1988. Increased light interception leads
yield deficit
to increased plant photosynthetic activity, which
Ryegrass
would affect C assimilation as well as other plant
Below ground 77.50
37.90 24.25
metabolic processes such as water use, mineral
Above ground 7.99
23.02 2.16
uptake and N fixation.
Total 21.71
35.03 6.61
The severe reduction in DM yield, especially
White clover
leaf growth, observed for white clover grown in
Below ground 31.00
12.24 2.00
shoot+root interaction treatment at severe soil
Above ground 1.19
71.14 4.19
water deficit compared with shoot interaction treat-
Total 2.20
69.52 4.13
Petriole 8.49
72.48 3.09
ment Table 1 may be due to several factors.
Leaf lamina 1.03
50.09 4.02
First, at severe soil water deficit, white clover is
Leaf total 1.55
16.87 3.28
unable to reduce either relative canopy conduc-
Stolon 6.78
45.45 1.70
tance or rate of leaf transpiration as efficiently as ryegrass and, therefore, is not as well adapted as
Significant at P=0.01. Significant at P=0.001.
the grass companion to avoid the effects of severe
176 D.W. Lucero et al. European Journal of Agronomy 11 1999 167–177
white clover to reduction in the N fixing capacity in shoot+root interaction. Ryegrass increased
of nodules and noted that the severity of nodule shoot biomass yield can be attributed to benefits
response depended on the length and degree of the from white clover’s N fixing ability, whereas the
water stress. In our study, the 37 day period of causes for increased white clover biomass yield
water stress at the plant level would have been of need to be studied further. However, at severe soil
sufficient length to have led to the reduction in the water deficit, ryegrass had a competitive advantage
N fixing capacity of white clover nodules. Butler over white clover when grown in shoot+root inter-
and Ladd 1985 found a direct decrease in action. This was due to the larger root system of
Medicago N fixation due to ryegrass competition ryegrass and its ability to control transpirational
and indicated that N fixation was directly related losses more efficiently, thus prolonging its growth
to legume weight. In our study, the DM yield of period compared with white clover.
white clover grown in shoot+root interaction with To explain these findings more fully, studies are
ryegrass at severe soil water deficit was 60 of
needed that look at the influence of white that when grown in shoot interaction with ryegrass.
cloverryegrass root interaction on 1 plant soil In addition, the increased DM yields observed in
carbon allocation, and 2 the plant use of soil ryegrass grown in shoot+root interaction with
resources other than water. white clover at no and moderate soil water deficit
levels was not observed at severe soil water deficit,
Acknowledgements
which further indicates that N fixation by white clover was most probably reduced by severe soil
The first author was supported as an American water deficit. Butler and Ladd 1985 additionally
Fulbright Scholar in France by the Franco– noted that during plant competition the observed
American Commission for Educational Exchange, increases in the DM yield of ryegrass were directly
to whom thanks are due. Additional appreciation related to an equal percentage decrease in the
is extended for funding received from the Integrated amounts of fixed N by the companion clover. The
Program GALILEE, a Franco–Italian collabora- reduced DM yield of white clover observed in our
tion partially funded by the Ministe`re Franc¸ais des experiment at severe soil water deficit would not
Affaires Etrange`res. The authors are very grateful only have decreased the capacity of white clover
for the tremendous help given by all Ph.D. students to fix N, but further allowed ryegrass to become
and technical staff of the Laboratoire Agronomie much more aggressive for limited available soil
et Environnement, ENSAIA, Nancy, France, as water. In our experiment at severe soil water
well as innumerable others who helped in the deficit, white clover made up only 31
of the measurements and harvests.
shoot canopy DM yield at harvest when grown in shoot+root interaction with ryegrass, whereas
when grown in no interaction or in just shoot
References
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, respectively. Thus, as soil water deficit increased,
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water limiting conditions for white clover and
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branching to growth of plant leaf area under water deficit
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5. Conclusion
