Soil Eiol. &&em. Vol. 25, No. 2, pp. 157-164, 1993 0038-0717/93 S6.00 + 0.

00
Printed in Great Britain. All rights resewed Copyright 0 1993 Peqamon Press Ltd

INVOLVEMENT OF SOIL ABIOTIC FACTORS IN THE

MECHANISMS OF SOIL SUPPRESSIVENESS TO
FUSARIUM WILTS
HAMID AMIR and CLAUDE ALABOWETTE*
I.N.R.A., Laboratoire de Recherches sur la Flare Pathog&e et la Faune du Sol, BV 1540,21034, Dijon
Cedex, France

(Accepted 25 Augusf 1992)

Summary-Two soils from Algerian palm groves were chosen for their abiotic characteristics. The soil
from B&ni-abb& contains: sand 96% and clay 2.5%; the soil from Tolga: clay 37%, silt 44%, sand 19%.
When infested with Fusarium oxysporum f.sp. iini the sandy soil appeared conducive and the clay soil
suppressive to fusarium wilt. After addition of glucose the kinetics of CO, released was faster and greater
in the suppressive than in the conducive soil. Study of the population dynamics of an introduced
population of F. oxysporum f.sp. lini showed that the inoculum density decreased faster and to a lower
threshold in the conducive than in the suppressive soil. Suppressiveness of this soil was not related to poor
survival of the inoculum.
Addition of clay, talc or humus to the sandy soil improved the survival of the pathogen, the mixture
clay plus humus enabling the survival of 97% of the introduced population. But addition of montmoril-
lonite or talc to this sandy soil resulted in an opposite effect on the kinetics of CO, release after glucose
amendment. The amount of CO, released was greater after addition of montmo~llonite and lower after
addition of talc than in the non-lends control. Similarly, talc and montmo~Ilonite had en opposite
effect on the level of soil suppre~iveness to fusarium wilt. Montmorillonite made the soil more suppressive
and talc more conducive than the non-amends control.
These results showed that modifications of the texture of a sandy soil by addition of clay may induce
changes of microbial activity resulting in modification of several properties of the soils: the ievel of
fungistasis and the suppressiveness of the soil are not independent of the soil texture.

tNTRODUCtlON biotic factors in the mechanisms of suppression.

As early as 1892 Atkinson, describing fusarium wilt
of cotton, indicated that disease severity varied
according to soil type. Walker and Snyder (1933)
studying fusarium wilt of pea in Wisconsin, and
Reinking and Manns (1933) the Panama disease of
banana in central America, established that wilt
spread more rapidly in sandy soils than in soils of
finer texture. Stotzky and Martin (1963) indicated
that suppressiveness of soil to fusarium wilt of ba-
nana was generally correlated with the clay content of
soil, particularly montmorillonitic clay. Further stud-
ies by Stotzky (1966) and Stotzky and Rem (1966)
demonstrated that smectite clays stimulate the
activity of the bacterial populations and therefore the
antagonism between bacteria and fungi in soil. How-
ever, the role of clays in relation to suppressiveness
of soils has never been clearly established and, as
stressed by Baker and Cook (1974), if fusarium wilts
are generally associated with sandy, acid soils, many
opposite situations exist.
Following the studies initiated by Komada and
Ezuka (1970), Arjunarao (1971) and Smith and
Snyder (1971, 1972) more recent research on soils
suppressive to fusarium wilt emphasized the role of
*Author for correspondence.
Louvet et al. (1976) demonstrated that the suppres-
siveness of the soil from Chsteaurenard disappears
after heat treatment of the soil for 30 min at 55°C and
Rouxel et al. (1979) showed the involvement of
non-pathogenic Fusariu~ in the mechanisms of
suppressiveness. Similarly Kloepper et al. (1980) and
Scher and Baker (1980) established the role of fluor-
escent pseudomonads in the mechanisms of suppres-
sion of fusarium wilt in soils from the Salinas Valley.
Finally, Alabouvette et al. (1985) demonstrated that
suppressiveness is also related to total microbial
biomass and activity which determines the intensity
of competition for nutrients between the pathogen
and the saprophytic microflora. However, it is obvi-
ous that the microbial balance in soil is not indepen-
dent of soil physico-chemical factors and it was
established that the efficiency of a selected antagonist
to control a disease depends on soil type (Paulitz et
al., 1990). Therefore the success of biological control
requires a better understanding of the interactions
between soil characteristics and microbial activity.
Amir (1991) characterized 40 soil samples from 10
different palm groves of Algeria and assessed their
level of receptivity to fusarium wilt of flax. These soils
differed in many physico-chemical properties and the
level of suppressiveness was correlated with salt con-
tent, but the soil texture also seemed to be involved.

157
158 HAMID AMIR
Amir et al. (1989) and Amir and Riba (1990) demon-
strated that a high salt content reduced the survival
of the pathogen in soil and therefore decreased the
inoculum potential of the soil. To study the influence
of texture, especially clay content, on disease suppres-
sion we compared pathogen survival and CO, pro-
duction after glucose amendment in a sandy
conducive soil and a suppressive soil with a higher
clay content. Finally the texture of a sandy conducive
soil was modified by addition of fine particles and the
consequences of these changes on suppressiveness
and other microbial properties were determined.
MATERIAL AND METHODS
Soil characteristics and soil amendments
The two soils, Tolga (Tol) and BCni-abbes (Ba),
were chosen among the most suppressive and the
most conducive soils to fusarium wilts after a survey
of 40 soils from 10 palm groves of Algeria (Amir,
1991). Their main characteristics are given in Table 1.
The water content at pF 1 was 33.5% (w/w) for To1
and 20.4% (w/w) for Ba. The experiments were
conducted at 60% of these values, i.e. 20% (w/w) for
To1 and 12% (w/w) for Ba.
The texture of the sandy soil Ba was modified by
addition of clay 25% (w/w), talc 25% (w/w) or humus
5% (w/w). The clay was a montmorillonite from
Greece having a cation exchange capacity (CEC) of
87 m-equiv 100 gg’ and a large surface area (750 m2
g-l). The clay particles had a ribbon-like microstruc-
ture and a size <2 pm. The talc had a CEC not
exceeding 1 m-equiv 100 g-‘; the powder chosen for
this experiment was made from platelets having a size
< 50 pm; the specific area was 3.5 m2 g-i. It was used
to modify the texture of the soil without affecting the
chemical properties of the clay.
Humus was also used to modify the texture of the
soil by introducing a fibrous material. It was made
from a brown peat extracted from Arandon (France).
It was heat-treated for 1 h at 120°C in the autoclave
to kill the microflora and then rinsed for several
hours under tap water to remove soluble carbon.
The amendments were mixed thoroughly with the
soil using a special device (“Turbula” type TlOB,
Maschinen-Fabrik Basel, Switzerland). Taking into
account the modification of the texture due to the
addition of 25% (w/w) of fine particles, the soil Ba
Table 1. Main characteristics of the two soils
B&i-abbk
Clay CO.002 mm (%) 2.50
Silt (fine) 0.002-0.020 (%) 0.30
Silt (coarse) 0.020-0.050 (%) 1.20
Sand (fine) 0.050-0.200 (%) 83.10
Sand (coarse) 0.200-2 (%) 12.90
Organic carbon (%) 0.23
Total CaCO, (%) 2.10
C/N 12.10
PH 8.80
Conductivity (mmho cm-‘) 0.43
and CLAUDE ALABOW
amended with clay or talc was watered to 20% (w/w).
The soil amended with humus as the control were
watered to 12% (w/w). Before being used, the
amended soil samples were kept for 3 weeks at
18-22°C. As the pH of the Ba soil is well buffered, the
amendments did not induce significant changes; the
greatest modification was registered after addition of
humus, the pH decreased to 8.3 in comparison to 8.7
in other treatments.
Fusarium strain and inoculum production
To monitor the population dynamics of F. oxyspo-
rum f.sp. lini in soil, a benomyl-resistant strain was
used. A microconidial suspension was U.V. irradiated
(254 nm) for 2 min and a resistant strain was selected
on PDA medium enriched with 10 mg benomyl 1-i.
This single spore isolate, called Foln35, showed the
same growth kinetics as the wild strain in sterilized
soil and was equally pathogenic on flax.
To produce the inoculum, the fungus was grown in
a malt extract liquid medium (10 g 1-l) in a 250 ml
flask on a rotary shaker at 125 rev min-’ at 25°C
under daylight. Ten-day old cultures were centrifuged
(3OOOg, 15 min) to remove the growth medium. The
propagules, mainly microconidia, were resuspended
in sterile distilled water and mixed with talc (1 ml of
conidial suspension in 2 g of talc). The paste made of
talc and inoculum was dried at 20°C by forced air, the
powder was then sieved ( < 200 pm) and stored dry at
4°C.
The concentration of viable propagules in talc was
determined by culture on malt agar following the
suspension-dilution technique. Three suspensions
were made by addition of 1 g of talc in 99 ml of sterile
water and 10 Petri dishes were poured with 1 ml of a
suitable dilution to obtain 20-60 colonies per dish.
The inoculum density resulted from the mean of these
three replicates of 10 Petri dishes.
Assessment of soil suppressiveness to fusarium wilt
To assess the suppressiveness of the soils, talc
inoculum of Foln35 was introduced at the initial
concentration of 40 x lo3 cfu gg’ soil. The exper-
iment was done in 12cm dia plastic pots with six
replicates. A susceptible cultivar of flax was seeded
and after emergence the seedlings were thinned to 10
per pot. Plants were grown in a greenhouse, under
daylight at 20-25°C and were watered daily. The
number of wilted plants was recorded weekly from
weeks 3 to 14 after planting.
Regression lines between disease incidence and
Tolga time were calculated and the slopes were compared by
37.20 the test proposed by Dagnelie (1975). Regression
33.30 lines were calculated without any transformation,
10.70
16.60 because the transformations tested (logit, log l/l-x)
2.50 did not improve the relationship.
2.18
28.20 Population dynamics of Foln35 in soil
9.40
7.90 Talc inoculum of Foln35 was mixed with the soils
2.17
at the initial concentration of 50 x 1O’cfu g-’ soil.
 Soil suppressiveness to fusarium wilts
The soil water content was then adjusted to 12% for
I&i-abbes and 20% for Tolga.
Three replicate soil samples of 100 g were infested
and kept in aluminium jars at 25°C for 60 days. After
3, 7, 14, 21, 28, 49 or 60 days the inoculum density
of each sample was determined from a 5 g subsample
of soil suspended in 45 ml of sterile water and shaken
for 15 min. Appropriate series of lo-fold dilutions
were prepared and aliquots of 1 ml were incorporated
in malt agar medium enriched with citric acid (250 mg
I-‘). benomyl(5 mg 1-l) and pentachloronitrobenzene
(100 mg 1-l). One subsample was taken from each
aluminium jar and 10 plates were poured for each
dilution. Colony numbers were determined after 96 h
at 25°C. Soil moisture was determined and the
inoculum density was expressed as number of cfu
g -’ of oven-dry soil. Inoculum densities (means of
three replicates) were compared after logarithmic
transformation by analysis of variance and
Newman-Keuls test.
Measurement of CO2 release from soil
Air dried soil samples were watered to 10% (w/w)
for Ba and 18% (w/w) for To1 and Ba amended with
clay or talc and kept at 25°C for 21 days to let the
microflora reach equilibrium. Subsamples of 100 g
were placed in flasks of 580 ml capacity. Three repli-
cate soil samples were enriched with glucose by
addition of 2 ml of a glucose solution containing 50 g
l-‘, corresponding to a final concentration of 1 mg
glucose g-’ of soil and a soil moisture content of 10%
and 20% (w/w). The flasks were sealed with a rubber
cap. One millilitre of the inert gas crypton was injected
into each flask as a standard to control the gas-tight-
ness of the flasks. The soil samples were kept at 25°C
and at each sampling time 5 ml of the flask atmos-
phere was taken with a syringe and injected in a
vacuum sealed tube. After each sampling, the flasks
were opened and the atmosphere changed by injection
of forced air for 1 min into the flasks. After addition
of crypton, the flasks were sealed again and kept at
25°C until the next sampling. The tubes with the
atmosphere samples were stored at 4°C until analysis
of the CO, concentration. CO, determination was
carried out by a gas chromatograph with a catharom-
eter as a detector. Chromatographic conditions were:
stainless steel column length 4.5 m, i.d. 3 mm, filled
with Porapak Q loo-120 mesh, oven temperature
4O”C, injector temperature 1 10°C detector tempera-
ture 110°C. Data were expressed as nmol CO, gg’ of
soil h-l. The amounts of CO2 released (mean of three
replicates) were compared by analysis of variance.
All the experiments were done at least twice with
similar results.
RESULTS
Suppressiveness of the soils
The percentage of diseased plants reached 55.9%
after 12 weeks of culture in the conducive soil from
159
B&i-abbes (Fig. 1). On the contrary, the percentage
of wilted plants remained low (11.8%) in the suppres-
sive soil from Tolga.
Regression lines between disease incidence and
time were calculated. The equations are:
y = 7.0x - 35.2 for Ba and y = 1.0x - 1.8 for Tolga;
the slopes are significantly different (P = 0.01).
Respiration rate of the soils after glucose amendment
After addition of 1 mg glucose gg’ soil, the kinetics
of CO2 release from the two soils were different
(Fig. 2). The initial respiration rate recorded after
1.5 h was 5.4 times higher in the suppressive soil than
in the conducive soil. In the suppressive soil, the
respiration rate increased quickly, reached its maxi-
mum after only 6 h, then decreased sharply and
dropped below the initial level after 24 h. On the
contrary, in the conducive soil the amount of CO2
released increased slowly, reached its maximum after
18 h, did not drop quickly and remained higher than
the initial rate for at least 48 h. The statistical analysis
revealed that the amount of CO2 released was signifi-
cantly higher in the suppressive than in the conducive
soil for 18 h, and then became significantly lower for
the rest of the experiment (P = 0.05). Moreover, the
total amount of CO* released from the suppressive
soil was greater than the amount released from the
conducive soil (P = 0.05).
Population dynamics of Fusarium in the soils
Following the introduction of 50 x 1O’cfu g-’ of
soil, the inoculum density of Foln35 dropped clearly
in both soils. However the kinetics of the population
decline was different in the two soils (Fig. 3). In the
conducive soil, the inoculum density decreased con-
tinuously for 20 days and seemed to stabilize at about
60
a
50
10
345678 9 10 11 12
Weeks
Fig. 1. Receptivity of Beni-abb& and Tolga soils to
fusarium wilt of flax: percentage of wilted plants after
infestation with F. oxysporum Esp. lini (40 x 103cfu g-’ of
soil). Treatments with the same letter are not significantly
different (P = 0.01).
160 HAMID At.n~ and CLAUDE ALABOUVETTE

l Coatrol
800 r- +
0 + Clay
+ t Humus
700 + + Humus + Clay
100
r x + Talc

0.1 L 11 28 42 60

100
0 w/w), clay (25% w/w) or clay and humus mixture to Ba soil
1.5 6 12 18 24 30
Hours
Fig. 2. Kinetics of CO2 release from Ba and To1 soils after
addition of 1mg of glucose g-l of soil.
7.3 x l@cfu g-’ soil corresponding to only 12% of
the initial inoculum density. In contrast, in the sup-
pressive soil, after an initial decrease, the inoculum
density stabilized at ca 40 x lo3 cfu g-l until day 30
of incubation and then dropped again. But after 60
days the inoculum density still represented 44% of
the initial population. At the end of the experiment
the inoculum densities in the two soils were
significantly different (P = 0.01).
Effect of the modification of the soil texture on the
population dynamics
In the non-amended control, the inoculum density
dropped regularly as establish~ previously in this
150 r
Days
Fig. 4. Effect of addition of humus (5% w/w), talc (25%
36 42 48
on the survival of F.oxysporwn f.sp. Miniintroduced at the
initial concentration of SOx lo3 cfu g-’ of soil (logarithmic
scale). Data with the same letter are not significantly
different (P = 0.05). Percentages are the amount of inocu-
lum after 60 days expressed as a percent of the initial
inoculum density.
soil from B&i-abbts (Fig. 4). After addition
of humus, the inoculum density also decreased
regularly, but remained at a level significantly higher
than in the control. Introduction of either mont-
morillonite or talc resulted in a better survival of
the pathogen; its density remained almost stable
for 30 days, then dropped slightly and after 60
days of incubation the inoculum density repres-
ented 41 and 43%, respectively, of the introduced
population.
The greatest survival of the pathogen was recorded
when the soil was amended with the mixture of clay
and humus; after 60 days the population density was
97% of the original and not significantly different
from that at the beginning of the experiment.

500
a

400 \
7f $
\
‘? r ’ \
‘M ’ .\
PI 300 -
’ t
8
Q 15
z
; 200

P
z”
15% 100
I I
5” ” ’
0 3 7 14 21 28 49 60
Days
Fig. 3. Kinetics of survival of F. oxysporum f.sp. lini in Ba
01 l
5 9
“1
15 1821
’
27
I
36
f
48
and To1 soils (logarithmic scale). Initial concentration:
Hours
50 x 10”cfu g-’ of soil. Data with the same letter are not
significantly different (P = 0.01). Percentages are the Fig. 5. Modification of the kinetic of CO* release from Ba
amount of inoculum after 60 days expressed as a percent of soil amended with glucose (1 mg g-l) following the addition
the initial inoculum density. of talc (25% w/w) or clay (2S% w/w).
 Soil suppressiveness to fusarium wilts
E$ect of modzjkation of soil texture on the respiration
rate
Following the addition of either montmorillonite
or talc, the kinetics of CO* release from the conducive
soil amended with glucose was changed (Fig. 5). In
the control, as previously established, the respiration
rate increased slowly, reached its m~imum after 18 h
and decreased slowly but remained higher than the
initial rate for 48 h. After addition of talc, the kinetics
of the respiration followed a curve similar to that of
the control, but the amount of CO, released was
always significantly lower than in the control. In
contrast, after amendment with montmorillonite, the
respiration increased more rapidly than in the control
and its maximum reached after 21 h corresponded to
an amount of CO2 twice that of the control. There-
after, the respiration rate decreased quickly but re-
mained higher than in the control until the end of the
experiment, when it was slightly less.
Effect of modi~cation of soil texture on the level of
suppressiveness
Figure 6 shows that addition of montmorillonite or
talc to the conducive soil induced changes in its level
of suppressiveness. Introduction of talc resulted in a
clear increase of disease incidence in comparison to
the non-amended control. In contrast, addition of
montmorillonite reduced wilt incidence that stabil-
ized at only 17.6% of wilted plants after 14 weeks of
culture. Calculation of the regression lines between
disease incidence and time shows that the slopes are
significantly different (P = O.OS),the equation being:
y =4.3x - 24.7 for Ba, y = 5.8x - 21.4 for Ba
amended with talc and y =2.4x - 15.5 for Ba
amended with montmorillonite.
Weeks
Fig. 6. M~i~~ations of Ba soil receptivity to fusarium wilt
of &x induced by cfay or talc amendments (25% w/w).
Percentage of wilted plants after soil infest&ion with F,
oxy.s~r~ f.sp. hi (40 x Iof cfu g-l of soil). Treatments
with the same letter are not significantly different (P = 0.05).
161
DISCUSSION
It has been clearly established that suppressiveness
of soil to fusarium wilts resulted from antagonistic
interactions between the pathogen and all or a
part of the saprophytic microflora (Alabouvette,
1990). However, it is clear also that the microbial
balance is partly under the control of the physical
and chemical characteristics of the soil (Baker and
Cook, 1974) and correlations were established
between suppressiveness and clay content of the
soils by Stotzky (1973). But it is difficult to manip
ulate the soil abiotic factors to demonstrate exper-
imentally their involvement in the mechanisms of
suppression. Indeed, the main characteristics of a
soil are not independent from each other, therefore
modification of one factor such as clay content may
result in changes of several properties of the soil
such as cation exchange capacity, pore sizes and
aggregation. However, in our study, we deli~rately
chose to modify the texture of a sandy soil by
addition of fine particles such as talc and montmoril-
lonite and to follow the induced changes in several
microbial characteristics of the soil. The results
demonstrate that addition of 25% of montmoril-
lonitic clay into the wilt-conducive sandy soil from
B&ii-abbes resulted in a better survival of the patho-
gen, an increased respiration rate after glucose
amendment and a higher level of suppressiveness to
fusarium wilt.
The two soils from Tolga and Ben&abbes were
chosen as representative of the most suppressive
and the most conducive soils after a survey of
40 different soils from southern Algeria. The
suppressive soil from Tolga is a clay loam with
37% clay; the conducive soil from B&i-abbes con-
tains only 2.5% clay and 1.5% silt. But these
soils also differed in several other abiotic character-
istics such as organic matter, calcium and salt con-
tents. The microbial biomass evaluated by the
method proposed by Chaussod et al. (1988) was 70
times smaller in the conducive soil than in the sup
pressive soil, which appeared low in comparison with
the values recorded in other soils (Chaussod et al.,
1988). This extremely smail biomass in the conducive
soil is related to its low content of organic matter as
well as of clay. There usually exists a correlation
between clay and organic matter contents, which
controls the amount of the biomass and its activity
(Chaussod et al., 1986).
The suppressiveness of the soil from Tolga and the
conduciveness of the soil from B&i-abbes appeared
clearly after 13 weeks of flax culture, in the soils
infested with F. oxysporum f.sp. hi. However the low
incidence of the disease in the suppressive soil is not
related to the destruction of the pathogen. On the
contrary, the study of the ~pulation dynamics
showed that the inocuhun density dropped faster and
to a lower concentration in the conducive than in the
suppressive soil. It has already been demonstrated
162 HAMIDAtm and CLAUDEALALIOUWTE
that the pathogen survives well in soils suppressive to
fusarium wilts (Scher and Baker, 1982; Alabouvette
et al., 1984).
Our study demonstrates that conduciveness is not
necessarily correlated with the establishment of the
pathogen at a high concentration. In the soil from
B&i-abbes, the pathogen was efficient even at a low
inoculum density. These results are in agreement with
observations showing that the total population of
F. oxysporum, and therefore the inoculum density of
the pathogen, is always very low in palm groves soils
(Amir et al., 1985). Indeed, according to Lockwood
(1988) inoculum density is only one of the factors
determining the soil inoculum potential, and in the
conducive soil, the environmental factors induce a
high inoculum potential even in the presence of a low
inoculum density.
The better survival of the pathogen in the suppres-
sive soil from Tolga seems related to its higher clay
and organic matter content than the conducive soil
from B&i-abbes. Similar results were recorded by
Amir (1991) studying the behaviour of F. oxysporum
in 40 different soil samples; the survival of the
pathogen was correlated with the texture of the soils
but not correlated with their level of suppressiveness.
Toussoun (1975) established that suppressive soils of
high clay content supported large populations of
F. oxysporum. This correlation between texture of the
soils and survival of F. oxysporum is confirmed by our
data showing that addition of humus, talc or mont-
morillonite to the sandy conducive soil resulted in
better establishment of the inoculum with talc and
montmorillonite having the greatest effect. In fact,
the inoculum density remained almost stable for 60
days, and an analysis performed 225 days after soil
infestation showed that in the soil amended with
montmorillonite the inoculum density stabilized at
46% of the introduced inoculum concentration, in
comparison with 0.4% in the control. Addition of
25% of clay to the sandy soil enabled the survival of
the pathogen similar to that in the soil from Tolga
which contains 37% of clays. These results are also
similar to those obtained by Couteaudier and
Alabouvette (1990) in a sandy loam with 5% of clays.
The added supplements did not provide energy to
the pathogen, even in the case of humus which was
used after sterilization and washing to eliminate the
soluble carbon. Therefore, the beneficial effect of talc,
clay or humus must be related to modification of the
soil texture; talc and montmorillonite have a smaller
particle size than the organic matter used in this
experiment. Interactions between clays and microor-
ganisms have been reviewed by Stotzky (1973), Baker
and Cook (1974), and Hattori and Hattori (1976).
Microorganisms can be adsorbed at the surface of
clay particles which form aggregates that protect
microorganisms from environmental stresses such as
desiccation. The clays can also adsorb substances
produced by microorganisms that are toxic for the
pathogen (Filip, 1973; Campbell and Ephgrave,
1983). All these properties of clays can contribute to
the better survival of the pathogenic Fusarium in the
sandy soil amended with montmorillonite. Reisinger
et al. (1977) proposed the coating of blastospores of
Beauveria bassiana with clay to improve their survival
in soil.
Amendment of the sandy soil with talc and mont-
morillonite also modifies the activity of the microflora
as assessed by measuring the rate of glucose mineral-
ization. After addition of 25% of montmorillonite the
kinetics of CO, released from the soil from
B&ii-abbes became similar to that of the suppressive
soil from Tolga. The dynamics of glucose mineraliz-
ation in the suppressive soil is characterized by three
features: (1) an initial respiration rate higher than
that in the conducive soil, reflecting a greater initial
biomass; (2) a rapid increase of the respiration rate
indicating that the biomass is immediately utilizing
the available nutrients; (3) an early and sharp decline
in CO, release corresponding to the cessation of the
microbial development following the nutritional
stress which accompanies equilibration of the microfl-
ora with the new energy state of the soil.
These three phases [already described by
Alabouvette et al. (1985a) in another suppressive
soil], indicate that the microbial biomass in the
suppressive soil is greater and more responsive to
energy-yielding nutrients than the biomass of the
conducive soil. Consequently, competition for nutri-
ents is more intense in the suppressive than in the
conducive soil, thus limiting the possibilities for
development of microorganisms, especially patho-
genic F. oxysporum (Alabouvette et al., 1985b). Ac-
cording to Cook and Baker (1983) this phenomenon
corresponds to “general suppression”, the inhibition
of the pathogen being related to the total amount of
microbial activity acting as a nutrient sink.
Addition of talc or montmorillonite have opposite
effects on the respiration kinetics of the sandy soil
and on the suppressiveness of this conducive soil.
Addition of talc reduced the respiration rate after
glucose amendment and made the soil more condu-
cive to the disease. In contrast, montmorillonite
enhanced the respiration rate of the soil as well as its
level of suppressiveness. These effects of montmoril-
lonite could be related to the stimulation of the
metabolism of bacteria, established by Stotzky
(1966), who attributed this stimulation to the in-
creased cation exchange capacity, because of the large
surface area of the clay. However, this demonstration
was established in vitro and there is no clear expla-
nation of the mechanisms by which montmorillonite
induces increased suppressiveness in field soils.
The observation that montmorillonite stimulated
microbial respiration in the conducive soil and also
increased its suppressiveness demonstrates that these
two phenomena are correlated and reinforces pre-
vious findings that suppressiveness of soil to fusarium
wilts is related to the activity of the saprophytic
microflora. Our results also demonstrate that there is
 Soil suppressiveness to fusaiium wilts
no clear relationship between the capacity of the soil
to support the survival of the pathogen and its level
of suppressiveness. These observations are not con-
tradicto~ to each other. Certain concepts associated
with the ecology of soil-borne plant pathogens
(Lockwood, 1988) help with the interpretation of
these data. We propose that in the sandy soil, a low
content of organic matter and consequently the lack
of carbonaceous nutrients available for the micro-
organisms induces exudation of nutrients from the
fungal propagules that are debilitated before being
lysed (Lockwood, 1990). This phenomenon can ex-
plain the poor survival of the pathogen when intro-
duced into the conducive soil from B&i-abbes. In
contrast, in the suppressive soil, a larger biomass is
responsible for a more intense competition for nutri-
tion inducing a stronger fungistatic effect than in the
conducive soil. The fungistasis inhibits the germina-
tion of the fungal propagules and favours the survival
of the inoculum (Lockwood, 1981). In the conducive
soil, the smaller microbial biomass is less restrictive
of the germination of the surviving propagules of the
pathogen, in the close vicinity of the plant root tip
where exudates provide energy-yielding nutrients.
Thus a low inoculum density is sufficient to provide
for infection of the plants.
This interpretation of our data fits with other
results obtained by Filonow and Lockwood (1983)
showing that sandy soils had a greater nutrient sink,
as measured by CO2 evolution, than finer-textured
soils.
These mechanisms of general suppression are not
contradictory to the role of specific populations of
microorganisms inhibiting the growth of the patho-
gen. (Cook and Baker, 1983). It has been demon-
strated that non-pathogenic Fnrsarium(Rouxel et at.,
1979), fluorescent Pseudomonas (Scher and Baker,
1982) and actinomycetes (Amir and Amir, 1989) also
play a role as antagonists of the pathogen.
Our study demonstrates that these microbial inter-
actions are not independent of the abiotic environ-
ment in which they take place. It demonstrates that
changing the texture of a sandy soil by addition of an
active clay enhances microbial activity and suppres-
siveness of the soil. The role of high soil pH was
investigated by Scher and Baker (1980) in relation to
the antagonism between fluorescent pseudomonads
and F. oxysporunt; Amir and Riba (1990) demon-
strated that high salt contents in saharian soils
provoke the destruction of the pathogenic Fusarium.
All these studies demonstrate the complexity of the
phenomenon of soil suppressiveness to fusarium wilts
which is based on many interactions between the soil
abiotic factors and the microflora on one hand and
between the pathogen and the saprophytic or antag-
onistic microflora on the other hand. All these results
also show that it is not possible to classify soils
strictly as either suppressive or conducive to fusarium
wilts; it is clear now that a continuum exists between
soils strongly suppressive to soils highly conducive
163
and that either a biotic or an abiotic change may
modify the level of suppressiveness of the same soil.
Therefore it could be useful to consider not the
supp~siveness but the receptivity (Ala~uvette
et al., 1982) or the receptiveness (Linderman et al.,
1983) of soils to microorganisms.
Acknowledgements-The authors are thankful to Dr R.
Chaussod for measurement of soil microbial biomass and to
Professor J. L. Lockwood for helpful criticism of the
~nu~~pt.
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