Applied Soil Ecology 18 (2001) 229238

Use of soil enzyme activities to monitor soil quality in natural and

improved fallows in semi-arid tropical regions
Ndour Ndye Yacine Badiane a,b , J.L. Chotte a, , E. Pate a , D. Masse a , C. Rouland c
a

Laboratoire de Bio-Pdologie, IRD, BP 1386 Dakar, Senegal

b Universit Cheikh Anta Diop, BP Dakar, Senegal
Laboratoire dEcophysiologie, Universit Paris XII, Val de Marne, 94010 Crteil Cedex, France
Received 29 January 2001; received in revised form 3 July 2001; accepted 6 July 2001

Abstract
Soil enzyme activities (-glucosidase, amylase, chitinase, xylanase) were investigated in natural and improved fallows of
the semi-arid zone of Senegal. The effect of age (4-, 11-, and 21-year-old), management (fenced versus grazed), and vegetation
(natural, Acacia holocericea, Andropogon gayanus) were compared. Principal component analysis revealed a relationship
between enzyme activities and the age and the management of fallows. -Glucosidase and amylase activities were significantly
higher in the oldest natural fallows. The highest xylanase activity was recorded for the A. gayanus improved fallows. This
fallow also showed highest chitinase activity, similar to that of the 21-year-old natural fenced fallow. Amongst the different
types of fallow management studied, the introduction of A. holocericea depleted all the tested activities. No relationships
between enzymes activities and soil organic content, and total microbial biomass were evident. The reasons for the observed
variations are discussed. 2001 Published by Elsevier Science B.V.
Keywords: Fallows; Agricultural practices; Enzymes activities; Soil organic matter; Microbial biomass

1. Introduction
In western African savanna, forest fallows have
been overexploited due to the removal of firewood
and overgrazing, and their duration has been shortened because of demographic pressure (Floret and
Pontanier, 1993). In Mali, Olsson (1984) indicated
that the average duration of the fallow period between
successive croppings has been reduced from 19 to 9
years during the past 10 years. Consequently, fallow
systems, based on the regeneration of natural vegetation leading to the restoration of soil properties (Nye
and Greenland, 1960; Laudelout and Van Bladel,

Corresponding author. Tel.: +221-849-33-08;

fax: +221-832-16-75.
E-mail address: chotte@ird.sn (J.L. Chotte).

1967) can no longer be thought of as efficient tools

to regenerate exhausted soils (Masse et al., 1998).
Though organic residues have a positive impact on
soil quality, their extensive use cannot be proposed
as a means to combat soil degradation because of a
general shortage of this type of material (Allard et al.,
1983). Therefore, the sustainability of African farming systems relies very much on the improvement of
natural fallows by the introduction of exotic and local
woody or herbaceous species (Cesar and Coulibaly,
1991; Dupuy et al., 1991), the aim being to restore
soil properties within a shorter period than is possible
using natural vegetation (Hoefsloot et al., 1993; Szott
et al., 1994).
The microbiological and biochemical status of the
soil has often been proposed as an early and sensitive indicator of soil ecological stress or restoration

0929-1393/01/$ see front matter 2001 Published by Elsevier Science B.V.

PII: S 0 9 2 9 - 1 3 9 3 ( 0 1 ) 0 0 1 5 9 - 7

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processes in both natural and agroecosystems (Martynuik and Wagner, 1978; Doran, 1980; Bolton et al.,
1985; Ramsay et al., 1986; Dick and Tabatabai, 1993;
Dick, 1994). Enzymes play a key role in soil nutrient
cycling. Enzyme activity in soil results from the activity of accumulated enzymes and from enzymatic activity of proliferating micro-organisms (Kiss et al., 1975).
Sources of accumulated enzymes are primarily microbial cells (Ladd, 1978), but they can also originate
from plant and animal residues (Bahl and Agrawal,
1972; Tabatabai, 1994). Enzymes accumulated in soil
are free enzymes such as exoenzymes released from
living cells, endoenzymes released from disintegrated
cells and enzymes bound to cell constituents (Kiss
et al., 1975). Numerous studies have been published
on the potential use of enzyme activity as an index of
soil productivity or microbial activity (Weaver et al.,
1994; Alef et al., 1995; Dick et al., 1996). The activities of some accumulated enzymes such as invertase,
-glucosidase and urease (Pankhurst, 1994) have all
been shown to be significantly higher in tilled soils
than in cultivated soils (Doran, 1980; Dick, 1984;
Gupta and Germida, 1988). These enzyme activities
are also higher in soils with crop rotations than in
monocultures (Dick, 1984; Miller and Dick, 1995).
This is why these enzymes were assumed to be accurate fertility indices (Skujins, 1978). Asparaginase
activity, bound to cell constituents and never accumulated outside cells (Mouraret, 1965), reflects soil organic content (Balicka and Sochacka, 1959). Other
enzymes, i.e. alkaline phosphatase and catalase, are
reported to be correlated with biotic factors because
they show a very close relationship with soil biomass
(Frankenberger and Dick, 1983; Seug et al., 2000).
In a recent study, Kandeler et al. (1999) indicated
a close relationship between enzyme activities and
particle-size fractions, with xylanase and invertase being associated with coarse sand, and the silt fraction,
respectively.
The present study is part of a research program
dealing with the impact of land management on soil
functioning in African farming systems. The objective
of this study was to evaluate the effects of different
fallow management practices on soil enzyme activities. We hypothesised that their variations were more
likely to be a better indicator of soil quality than soil
organic matter content, for soil low in organic matter
(Masse et al., 1998).

2. Materials and methods

2.1. Field site
The study was conducted in the Region of Nioro
du Rip at Sonkorong, Senegal (13 45 N, 15 40 W).
The climate is dry tropical and rainfall is confined to
the period from July to October with a mean annual
value of 600700 mm. The mean annual temperature
is 30 5 C. The natural vegetation is a shrub savanna
dominated by Combretum glutinosum and Guiera
senegalensis. Farming systems are characterised by
a biennial rotation of peanut and millet, without any
fertilisation (Diatta, 1994). The soil was described
(Maignien, 1965) as sandy and ferruginous Oxisol
(FAO, 1998). Soil (010 cm layer) properties are:
10% clay, 28% silt, 62% sand and pH (H2 O) 5.8.
2.2. Experimental design
Natural and improved fallows were selected. For
the natural fallows three plots (each ca. 20 m 30 m)
were chosen (Diatta, 1994):
a 21-year-old fallow fenced and protected against
cattle grazing, fire and wood gathering, referred to
as F21f;
a 21-year-old fallow grazed and unprotected, open
to public access, F21g;
a 11-year-old fallow grazed and unprotected, F11g.
For the improved fallows, an area (ca. 100 m
100 m) cropped for at least 20 years was selected and
fenced in 1994. Three replicate plots (each measuring 20 m 20 m) of the following treatments were
established over a 4-year period:
natural regeneration of fallow vegetation (F4f);
plantation of 2-month-old seedlings of Acacia holocericea (F4fAh), each plot consisting of five rows
(20 m length, 3 m width, and six plants in each row);
plantation of Andropogon gayanus plants (F4fAg),
each plot consisting of five rows (20 m length, 3 m
width, and 40 plants in each row).
2.3. Sampling design
Soils were sampled at the end of the dry season in
May 1997 and 1998 for the natural, and the improved

N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

fallows, respectively. Samples were collected from the

010 cm soil layer. For the natural fallows (i.e. F21f,
F21g and F11g) the samples were taken under the
tree canopy (referred to as c) and outside this zone
(referred to as oc). For each zone three sub-plots
were identified.
Six soil samples were taken from each sub-plot of
natural fallows and from each replicate of improved
fallows. Sub-samples were mixed and one analysis
was carried out for each of them. For microbial determination, samples were stored at field moisture content at 4 C. For organic carbon, they were air-dried
and ground (<200 m).
2.4. Analyses
2.4.1. Biomass C
Microbial biomass C (MB) of soil sub-samples (20 g
EDW) was determined by a fumigationextraction
method (Amato and Ladd, 1988), using ninhydrin-N
reactive compounds extracted from soils with 2 M
KCl after a 10-day fumigation period. Fumigated
and unfumigated soil samples were suspended in
KCl solution (1:3 dry soil/solution, w/v; 2 M final
concentration), shaken at 25 C for 1 h and then centrifuged for about 5 min (2000 g). Extracts were
filtered (0.45 m) and stored frozen pending further
analysis. Ninhydrin-reactive nitrogen was determined
from 0.5 ml of extract from each of the fumigated and
unfumigated soils. Aliquots were mixed with 1.5 ml
of 2 M KCl and 2.0 ml of freshly-prepared ninhydrin
reagent. Tubes were placed in a boiling waterbath for
15 min, cooled, and 5 ml of 50% ethanol were added to
each. Absorbances at 570 nm were calibrated against
standard solutions of l-leucine and ammonium sulphate. Biomass C = ninhydrin-N 21 (g g1 of dry
soil).
2.4.2. Organic carbon
Total organic carbon (C) of the soil sub-sample
was determined by potassium dichromate oxidation
(Walkey, 1935). Results were expressed as mg C g1
soil.
2.4.3. Enzyme activities
-Glucosidase activity was determined according
to a method adapted from Hayano (1973). Briefly,
100 mg of air-dried soil, was incubated for 2 h at 37 C,

231

with 100 l of 5 mM paranitrophenyl -d-glucopyranoside (Sigma), and 400 l of a citrate phosphate

buffer (MacIlvain, 1921) at pH 5.8. The reaction
was stopped with 3 ml of 0.2% Na2 CO3 (w/v). The
para-nitrophenol (PNP) released by -glucosidase
activity was measured at 400 nm (Ultrospec 3000,
Pharmacia Biotech). Results were expressed as
g PNP released g1 h1 . For the measurement of
chitinase activity in soil, the same method was used
with paranitrophenyl N-acetyl glucosaminide (5 mM,
Sigma) as the substrate.
For measuring amylase and xylanase activity,
300 mg of air dried soil was incubated with 1% (w/v)
xylan or starch and a citrate phosphate buffer at pH
5.8 (MacIlvain, 1921). Reducing sugar released during the incubation period (4 h) was measured using
Somogyi (1945) and Nelson (1944) reagents. Results
were expressed as g glucose g1 h1 .
2.4.4. Statistics
The effects of the different land management practices were tested by between-class principal component analysis (PCA) (Doldec and Chessel, 1994),
taking into account the different fallow types. This
multivariate analysis is based on the linear model of
variance analysis. It consists of decomposing the total variability between land management techniques.
Here, decomposition into six categories corresponding to samples from the fallows F21f, F21g, F11g,
F4f, F4fAh and F4fAg allows focusing on the variations in enzyme activities between different fallow
ages and management. A Monte Carlo test (Manly,
1991) was carried out to check the significance of differences in enzyme activity between the fallows. The
total between-class inertia is computed after random
permutations of the samples, and compared to the
initial (not permuted) between-class inertia. The software employed for between class PCA and the Monte
Carlo test was ADE-4 (Thioulouse et al., 1996). The
ADE-4 modules used were PCA (option: correlation matrix) and Discrimin (options: between-class
analysis and test).
To complement the between-class PCA, analyses
of variance were carried out on enzyme activities (Statview 4.02: ANOVA) to test differences
between fallows and treatments (F21f.c, F21f.oc,
F21g.c, F21g.oc, F11g.c, F11g.oc, F4f, F4fAh and
F4fAg).

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To test if the variations in enzyme activities were

related to differences in microbial biomass and the
soil organic carbon content, a PCA with respect to
instrumental variables (Lebreton et al., 1991) was
carried out with module projectors of the ADE-4 software (options: table orthonormal basis and PCA
on instrumental variables). A Monte Carlo test (module projectors, option: sub-space test) was carried out
to check the multivariate regression between enzyme
activities and the microbial biomass and the organic
carbon content. Univariate regression analysis was

carried out between the activity of each enzyme, and

the microbial biomass or organic carbon.

3. Results
3.1. Effects of fallow age and management
The inter-fallow analysis showed that 49.8% of the
variations in enzyme activities was explained by the
differences between the fallow plots. A random test

Fig. 1. Between-class PCA between fallows: effects of age and management practices: (A) eigenvalues bar chart; (B) first factor map for
fallows; (C) first factor map for enzymes.

N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

demonstrated that the inertia percentage was significant

(P < 0.0001), indicative of significant differences
between the activities recorded in the fallows.
The first axis (F1) of principal component analysis
expressed 71% of the inertia between fallows and the
following axis (F2) 21% (Fig. 1A). The combination
of these two factors reflected the variation in enzyme
activities according to fallow age and management.
Except for the A. holocericea treatment (F4fAh), protected fallows had positive coordinates along the F1
axis, while non-protected fallows presented negative
coordinates. Moreover, the old grazed natural fallow
under the tree canopy (F21g.c) clustered with the
fenced plots of similar age (Fig. 1B). These differences
resulted from higher chitinase and xylanase activities
in fenced fallows than those in grazed plots (Fig. 1C).
Along the second axis we observed a gradient
between age of fallows. Except for the natural grazed
fallow (outside the tree canopy, F21g.oc), old natural
fallows (F21f.c, F21g.c) presented negative coordinates along the F2 axis (Fig. 1B). By contrast, the
younger fallows (F4f, F4fAh, F4fAg, F11g.oc), except for the 11-year-old grazed fallow under the
tree canopy (F11g.c), presented positive coordinates.
Factor F2 indicated that -glucosidase and amylase
activities were generally higher in older fallows than
in younger fallows (Fig. 1C).
ANOVA showed that the -glucosidase activity
recorded in the old protected fallow (F21f) was higher
than in the younger fallows (P < 0.0315), i.e. F4fAh
and F11g.oc (Table 1). The fenced young fallow (F4f)
and the natural grazed fallow (F11g.c) had significantly higher -glucosidase activities than F11g.oc.
Amylase activities were significantly (P < 0.01)

233

higher under the tree canopy of natural old fallows

(F21f.c and F21g.c) than in fallows such as F11g.oc,
F4fAh and F4fAg. The highest chitinase activities
were recorded in the old protected natural fallow
(F21f), the old unprotected natural fallow under the
tree canopy (F21g.c), and in the A. gayanus treatment
(F4fAg). By contrast, the lowest activities were observed in the unprotected natural fallows (F11g.c and
F21g.oc). For the xylanase activity, values recorded
in protected improved fallows (F4f and F4fAg) were
significantly higher than those recorded in the grazed
natural fallows except for F21g.c (Table 1). For the
improved fallows, the xylanase activity was the highest in the A. gayanus plot (F4fAg).
3.2. Relationships between enzyme activity
and soil organic matter
The inertia of PCA (enzyme activity) on instrumental variables (microbial biomass and organic carbon)
represented 17.8% of the variation in enzyme activity
(PCA inertia). A random test showed that this inertia
percentage was significant (P < 0.01), indicative of
a significant relationship between enzyme activity
on the one hand, and microbial biomass and organic
carbon content on the other. The first axis expressed
clearly these relationships since it represented 97% of
the inertia of PCA on instrumental variables (Fig. 2A).
This factorial axis showed the positive relationships
between -glucosidase and amylase activities and
organic carbon content (Fig. 2B and C). This result
was confirmed by regression analysis, which indicated significant relationships between organic carbon
content and -glucosidase activity (P < 0.0018;

Table 1
Mean enzyme activities (g product g1 soil h1 )a
Fallow treatments

Sampling location

Code

-Glucosidase

Amylase

Chitinase

Xylanase

21-year-old natural fallow, fenced

21-year-old natural fallow, fenced
21-year-old natural fallow, grazed
21-year-old natural fallow, grazed
11-year-old natural fallow, grazed
11-year-old natural fallow, grazed
4-year-old natural fallow, fenced
4-year-old Andropogon fallow, fenced
4-year-old Acacia fallow, fenced

Under the tree canopy

Outside the tree canopy
Under the tree canopy
Outside the tree canopy
Under the tree canopy
Outside the tree canopy

F21f.c
F21f.oc
F21g.c
F21g.oc
F11g.c
F11g.oc
F4f
F4fAh
F4fA

78.73
70.14
61.44
40.26
64.84
37.12
65.07
46.13
54.00

5.57
3.42
4.96
2.78
3.45
1.82
3.23
2.37
2.83

40.39 a
34.72 ab
32.92 abc
25.41 bcde
19.7 cd
16.89 e
27.87 bcd
23.48 cde
35.64 ab

2.36
1.91
1.72
1.58
1.29
0.84
2.49
1.38
4.55

a
ab
bcd
cd
abc
d
abc
cd
bcd

a
bc
ab
c
bc
c
bc
c
c

Means within columns followed by the same letter are not significantly different (ANOVA, P < 0.05).

bcd
bcd
bcd
cde
de
e
b
de
a

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Fig. 2. Principal component analysis with respect to instrumental variables (PCAIV) between the table of enzyme activities and the table of
carbon and microbial biomass: (A) eigenvalues bar chart; (B) first factor map for enzymes; (C) first factor map for instrumental variables.

R = 0.6) and between organic carbon content and

amylase activity (P < 0.013; R = 0.46). Old fallows
had higher organic carbon content and higher activities of -glucosidase and amylase than young fallows
(Fig. 3A and B). No correlation was found between
chitinase and xylanase activities and carbon content
for any of the fallows. There was no significant relationship between enzyme activities and microbial
biomass content in fallows.

4. Discussion
-Glucosidase and amylase activities were significantly higher in 21-year-old than in 11-year-old
fallows. These enzymes have been detected in microorganisms, animals and plants (Bahl and Agrawal,
1972), but they are present also in toluene treated soil
(Hofmann and Hofmann, 1953, 1955), indicating that
they could be free extracellular enzymes (Skujins,

1976) adsorbed on the surface of soil particles (Hayano

and Katami, 1977). The exact origin, quantity and
quality of the organic substrates and/or the stimulation of specific microbial communities associated
with the observed high levels of -glucosidase and
amylase activities in the studied fallows cannot be deducted from this study. However, the positive impact
of soil cover and lack of tillage on these soil enzyme
activities has already been stressed by Gupta and
Germida (1988), Angers et al. (1993) and Deng and
Tabatai (1996). Their activity increases with organic
matter content (Doran, 1980; Miller and Dick, 1995)
and this is why they are considered as very sensitive
biological indicator of the effects of soil management
practices (Dick, 1994; Miller and Dick, 1995).
The correlation matrix showed a significant and
positive relationship between -glucosidase and amylase activities and organic carbon content, as already
pointed out by Eivazi and Tabatabai (1990). However,
our study was conducted on a sandy soil and the effect

N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

Fig. 3. Correlation between -glucosidase and amylase activities

and organic carbon content in fallows: (A) correlation between
-glucosidase and organic carbon content; (B) correlation between
amylase and organic carbon content.

235

of fallows on soil organic content was not as evident as

that recorded for heavy clay soils (Feller, 1994). Different levels of -glucosidase activity were recorded
in plots of similar soil carbon content. For fallows of
the same age (21-year-old) -glucosidase activity was
higher in the fenced plots than that in the grazed fallows, while organic carbon content was similar in both
plots. A similar conclusion can be drawn for amylase and xylanase activity. Many studies (Pancholy and
Rice, 1973a,b; Burns, 1978; Nannipieri et al., 1983)
have suggested that enzyme activity depends on the
quality of organic inputs. Herbaceous plants dominated the vegetation of young fallows, whereas woody
plants dominated in old fallows (Manlay et al., 2000).
This shift in vegetation cover may have had an impact
on the quality of organic inputs and could therefore
explain the differences in enzyme activities.
Chitinase activity in the A. gayanus plots and the
old protected fallows was significantly higher than in
the grazed plots. Chitin is a common structural substance and can be found in the cell wall of fungi
(basidiomycetes, ascomycetes) and insects. Some of
the chitinase activity in soil might be produced by
plant roots, as a reaction to fungal infection (Dixon,
1986; Kurosaki et al., 1986). The presence of chitinase
activity in old protected fallows and in A. gayanus
plots could be linked to the presence of a high fungal
biomass in these fallows.
Among the different management practices, the
introduction of A. holocericea reduced the activity of
every enzyme. High concentration of phenolic compounds (12 mg N as phenol g1 dry matter), responsible for growth inhibition of soil micro-organism
might explain this finding (Duponnois et al., 2001).
In this study, the authors recorded lower multiplication rates of nematodes, lower radial fungal
growth (i.e. Arthrobotrys oligospora) and lower microbial biomass in soils amended with enriched phenolic compounds (A. holocericea versus Sorghum
vulgare).
No relationship between enzyme activity and microbial biomass was recorded. For -glucosidase, this
appeared to be anomalous since this enzyme releases
important energy sources for soil micro-organism,
necessary for their development. However, biomass
estimations were performed at field moisture content
(<15% water holding capacity) on soil sampled at
the end of the dry season, whereas enzyme activities

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N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

were measured under optimal conditions. Thus, this

difference in soil moisture content may explain our
results. Moreover, the assayed enzymes may originate
from the activity of organisms other than microbial
biomass such as protozoan and invertebrates.

5. Conclusion
Soil enzymes were found to discriminate between
land management practices, and therefore appear to
be useful for monitoring changes in soil over time.
-Glucosidase was the most sensitive enzyme for
showing differences between fallows. However, no
clear relationship between enzyme activity and other
soil characteristics (carbon content, total microbial
biomass) were found. Quality of organic input (woody
versus herbaceous) may explain this finding. Further
research is needed to confirm this hypothesis, and the
role of enzyme activity in nutrient cycling in tropical
sandy soils.

Acknowledgements
This work received financial support from the Interinstitutional Inciting Action IRD-CNRS-CIRADINRA Bio-functioning of tropical soils and sustainable land management and from the EC Project
Reduction of the Fallow Length, Biodiversity and
Sustainable Development in Central and West Africa
(TS3-CT93-0220, DG12 HSMU) (Floret, 1998). The
authors are grateful to Dr. Jean Thioulouse for constructive suggestions.
References
Alef, K., Nannipieri, P., Trazar-Cepada, C., 1995. Phosphatase
activity. In: Alef, K., Nannipieri, P. (Eds.), Methods in Applied
Soil Microbiology and Biochemistry. Academic Paris, London,
pp. 335344.
Allard, J.L., Bertheau, Y., Drevon, J.J., Ganry, F., 1983. Ressources
en rsidus de rcolte et potentialits pour le biogaz au Senegal.
Agron. Trop. 38, 213221.
Amato, M., Ladd, J.N., 1988. Assay for microbial biomass based
on ninhydrin-reactive nitrogen in extracts of fumigated soils.
Soil Biol. Biochem. 20, 107114.
Angers, D.A., Bissonnette, N., Lgre, A., Samson, N., 1993.
Microbial and biochemical changes induced by rotation and

tillage in a soil under barley production. Can. J. Soil Sci. 73,

3950.
Bahl, O.P., Agrawal, K.M.L., 1972. -Galactosidases, -glucosidase, and -N-acetylglucosaminidase from Aspergillus niger.
In: Ginsburg, V. (Ed.), Methods in Enzymology, Vol. 28.
Academic Press, New York, pp. 728734.
Balicka, N., Sochacka, Z., 1959. Biological activity in light soils.
Z. Problem. Postep. Nauk. Rol. 21, 257265.
Bolton Jr., H., Alliott, L.F., Papendick, R.I., Bezdicek, D.F., 1985.
Soil microbial biomass and selected soil enzyme activities:
effect of fertilisation and cropping practices. Soil Biol. Biochem.
17, 297302.
Burns, R.G., 1978. History of abiotic soil enzyme research. In:
Burs, R.G. (Ed.), Soil Enzymes. Academic Press, London, 33
pp.
Cesar, J., Coulibaly, Z., 1991. Le rle des jachres et des cultures
fourragres dans le maintien de la fertilit des terres. In: Savanes
dAfrique, terres fertiles? Ministre de la Coopration et du
Dveloppement, Paris, pp. 271287.
Deng, S.P., Tabatai, M.A., 1996. Effect of tillage and residue
management on enzyme activities in soils. II. Glycosidases.
Biol. Fertil. Soils 22, 208213.
Diatta, M., 1994. Mise en dfens et techniques agroforestires au
Sine Saloum (Senegal). Effet sur la conservation de leau, du
sol et sur la production primaire. Thse de doctorat, Universit
de Strasbourg I, p. 202.
Dick, W.A., 1984. Influence of long-term tillage and crop rotations
combinations on soil enzyme activities. J. Am. Soil Sci. Soc.
48, 569574.
Dick, R.P., 1994. Soil enzyme activities as indicators of soil quality.
In: Doran, J.W., Coleman, D.C., Bezdicek, D.F., Stewart, B.A.
(Eds.), Defining Soil Quality for a Sustainable Environment.
Soil Sci. Soc. Am., Madison, pp. 107124.
Dick, W.A., Tabatabai, M.A., 1993. Significance and potential uses
of soil enzymes. In: Metting, F.B. (Ed.), Soil Microbial Ecology:
Application in Agricultural and Environment Management.
Marcel Dekker, New York, pp. 95125.
Dick, R.P., Breakwill, D., Turco, R., 1996. Soil enzyme activities
and biodiversity measurements as integrating biological
indicators. In: Doran, J.W., Jones, A.J. (Eds.), Handbook of
Methods for Assessment of Soil Quality. Soil Sci. Soc. Am.,
Madison, pp. 247272.
Dixon, R.A., 1986. Host antifungal agents. Nature 324, 303304.
Doldec, S., Chessel, D., 1994. Co-inertia analysis: an alternative
method for studying speciesenvironment relationship.
Freshwater Biol. 31, 277294.
Doran, J.W., 1980. Soil microbial and biochemical changes
associated with residue management with reduced tillage. Soil
Sci. Soc. Am. J. 44, 765771.
Duponnois, R., Chotte, J.L., Sall, S.N., Cadet, P., 2001. The
effect of organic amendments on the interactions between a
nematophagous fungus Arthrobotrys oligospora and the root
knot nematodes Meloidogyne mayaguensis parasitizing tomato
plants. Biol. Fertil. Soils, in press.
Dupuy, M., Detrez, C., Neyra, M., De Lajudie, P., Dreyfus, B.,
1991. Les acacias fixateurs dazote du sahel. La Recherche 233,
802804.

N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

Eivazi, F., Tabatabai, M.A., 1990. Factors affecting glucosidase
and galactosidase activities in soils. Soil Biol. Biochem. 22,
891897.
FAO, 1998. World reference base for soil resources. World Soil
Resources Reports, Food and Agricultural Organisation, Rome,
p. 98.
Feller, C., 1994. La matire organique dans les sols tropicaux
argile. 1. Recherche de compartiments organiques fonctionnels.
Une approche grannulomtrique, Doctorat dEtat, Strasbourg
Universit Louis-Pasteur, 393 pp.
Floret, C., Pontanier, R., 1993. Recherches sur la jachre en
Afrique tropicale. In: Floret, C., Pontanier, R., Serpenti,
G. (Eds.), La Jachre en Afrique Tropicale, Mab UNESCO,
pp. 1154.
Frankenberger, W.T., Dick, W.A., 1983. Relationships between
enzyme activities and microbial growth and activity indices in
soil. J. Am. Soil Sci. Soc. 47, 945951.
Gupta, V.V.S.R., Germida, J.J., 1988. Distribution of microbial
biomass and its activity in different soil aggregate size classes
as affected by cultivation. Soil Biol. Biochem. 20, 777786.
Hayano, K., 1973. A method for determination of -glucosidase
activity in soil. Soil Sci. Plant Nutr. 19, 103108.
Hayano, K., Katami, A., 1977. Extraction of -glucosidase activity
from pea field soil. Soil Biol. Biochem. 9, 349351.
Hoefsloot, H., Van Der Pol, F., Roeleveld, L., 1993. Jachres
amliores. Options pour le dveloppement des systmes de
productions en Afrique de lOuest.: Etude littraire. Royal
Tropical Institute, Dveloppement Agricole, 83 pp.
Hofmann, E., Hofmann, G., 1953. Occurrence of - and
-glycosidase in the soil. Naturwissenschaften 40, 511515.
Hofmann, E., Hofmann, G., 1955. The enzyme system of arable
soil. IV. Amylase. Z. Pflanzenernhr. Dng. Bodenkd. 70,
97102.
Kandeler, E., Stemmer, M., Klimanek, E.M., 1999. Response of
soil microbial biomass, urease and xylanase within particle size
fractions to long-term soil management. Soil Biol. Biochem.
31, 261273.
Kiss, S., Dragan-Bularda, M., Radulescu, D., 1975. Biological
significance of enzymes in soil. Adv. Agron. 27, 2591.
Kurosaki, F., Nobuhiko, T., Arasuke, N., 1986. Induction of
chitinase and phenyl-alanine ammonia-lyase in cultured carrot
cells treated with fungal mycelial walls. Plant Cell Physiol.
27, 15871591.
Ladd, J.N., 1978. Origin and range of enzymes in soil. In: Burns,
R.G. (Ed.), Soil Enzymes. Academic Press, London, pp. 5196.
Laudelout, H., Van Bladel, R., 1967. La jachre naturelle en
rgion tropicale humide. In: colloque sur la fertilit des
sols tropicaux. Tananarive, Madagascar, IRAT, Paris, 1925
November 1967, pp. 14901497.
Lebreton, J.D., Sabatier, R., Banco, G., Bacou, A.M., 1991.
Principal component and correspondence analyses with respect
to instrumental variables: an overview of their role in studies
of structureactivity and speciesenvironment relationships.
In: Devillers, J., Karcher, W. (Eds.), Applied Multivariate
Analysis in SAR and Environmental Studies. Kluwer Academic
Publishers, Dordrecht, pp. 85114.

237

MacIlvain, T.C., 1921. In: Sydeney, P., Colovick, N., Kaplan, O.

(Eds.), Methods in Enzymology, Vol. 1. Academic Press, New
York, 833 pp.
Maignien, R., 1965. Notice explicative; carte pdologique du
Senegal en 1/1000.000 ORSTOM, Dakar, p. 63.
Manlay, R.J., Cadet, P., Thioulouse, J., Chotte, J.L., 2000.
Relationships between abiotic and biotic soil properties during
fallow periods in the Sudanian zone of Senegal. Appl. Soil
Ecol. 14, 89101.
Manly, B.F.J., 1991. Randomization and Monte Carlo Methods
in Biology. Chapman & Hall, London, 281 pp.
Martynuik, S., Wagner, G.H., 1978. Quantitative and qualitative
examination of soil microflora associated with different
management systems. Soil Sci. 125, 340343.
Masse, D., Cadet, P., Chotte, J.L., Diatta, M., Floret, C.,
Ndiaye-Faye, N., Patte, E., Thioulouse, J., Villenave, C.,
1998. Jachres naturelles et restauration des proprits des
sols en zone semi-aride, Cas du Senegal. Agriculture et
Dveloppement 18, 3138.
Miller, M., Dick, R.P., 1995. Thermal stability and activities
of soil enzymes as influenced by crop rotations. Soil Biol.
Biochem. 27, 11611166.
Mouraret, M., 1965. Contribution lEtude de lActivit des
Enzymes du Sol: Lasparaginase. ORSTOM, Paris.
Nannipieri, P., Muccini, L., Ciardi, C., 1983. Microbial biomass
and enzyme activities: production and persistence. Soil Biol.
Biochem. 15, 679685.
Nelson, N., 1944. A photometric adaptation of the Somogyi method
for the determination of glucose. J. Biol. Chem. 153, 375380.
Nye, P.H., Greenland, D.J., 1960. The soil under shifting
cultivation. Technical Communications. CAB, Farnham Royal,
156 pp.
Olsson, K., 1984. Long-term changes in the woody vegetation
in North Kordafam, Sudan. A study with the emphasis on
Acacia senegal. Rapporter och Notiser, Lunds Universitets
Naturgeografiska Institution, Lund, 60 pp.
Pancholy, S.K., Rice, E.L., 1973a. Carbohydrases in soil as
affected by successional stages of revegetation. Soil Sci. Soc.
Am. Proc. 37, 227229.
Pancholy, S.K., Rice, E.L., 1973b. Soil enzymes in relation to old
field succession: amylase, cellulase, invertase, dehydrogenase,
and urease. Soil Sci. Soc. Am. Proc. 37, 227229.
Pankhurst, C.E., 1994. Biological indicators of soil health and
sustainable productivity. In: Greenland, D.J., Szabolcs, I.
(Eds.), Soil Resilience and Sustainable Land Use, pp. 331352.
Ramsay, A.J., Stannard, R.E., Churchman, G.J., 1986. Effects
of conservation from ryegrass pasture to wheat cropping on
aggregation and bacterial populations in a silt loam soil in
New Zealand. Aust. J. Soil Res. 24, 253264.
Seug, C., Rouland, C., Fall, S., Brauman, A., Mora, P., 2000.
Importance of earthworms casts and sheetings of some termite
species in different fallows (Kolda, Senegal). In: Floret, C.,
Pontanier, R. (Eds.), La jachre en Afrique Tropicale, Vol. II,
pp. 141149.
Skujins, J., 1976. Extracellular enzymes in soil. Crit. Rev.
Microbiol. 4, 383421.

238

N.N.Y. Badiane et al. / Applied Soil Ecology 18 (2001) 229238

Skujins, J., 1978. History of abiotic soil enzyme research. In:

Burns, R.G. (Ed.), Soil Enzyme. Academic Press, London,
pp. 149.
Somogyi, M., 1945. Determination of blood sugar. J. Biol.
Biochem. 160, 6168.
Szott, L.T., Palm, C.A., Davey, C.B., 1994. Biomass and litter
accumulation under managed and natural tropical fallows. For.
Ecol. Manage. 67, 177190.
Tabatabai, M.A., 1994. Enzymes. In: Weaver, R.W., Augle, S,
Bottomly, P.J., Berdicek, Q., Smith, S., Tabatabai, A., Wollum,
A. (Eds.), Methods of Soil Analysis. Part 2. Microbiological

and Biochemical Properties, No. 5. Soil Sci. Soc. Am.,

Madison, pp. 775833.
Thioulouse, J., Chessel, D., Doldec, S., Olivier, J.M., 1996.
ADE-4: a multivariate analysis and graphical display software.
Stat. Comp. 7, 7583.
Walkey, A., 1935. An examination of methods for determination organic carbon and nitrogen in soils. J. Agric. Sci. 25,
598609.
Weaver, R.W., Angle, J.S., Bottomley, P.S., 1994. Methods of Soil
Analysis. Part 2. Microbiological and Biochemical Properties,
No. 5. Soil Sci. Soc. Am., Madison.