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Soil Biology & Biochemistry 33 (2001) 205±214
www.elsevier.com/locate/soilbio

Response of soil food-web structure to defoliation of different plant
species combinations in an experimental grassland community
J. Mikola a,*, G.W. Yeates b, D.A. Wardle a, G.M. Barker c, K.I. Bonner a
a

b

Landcare Research, P.O. Box 69, Lincoln 8152, New Zealand
Landcare Research, Private Bag 11-052, Palmerston North, New Zealand
c
Landcare Research, Private Bag 3127, Hamilton, New Zealand

Received 14 January 2000; received in revised form 23 May 2000; accepted 20 June 2000

Abstract
We established a greenhouse experiment based on replicated mini-ecosystems to evaluate the effects of defoliation of different plant
species combinations on soil food-web structure in grasslands. Plant communities, composed of white clover (Trifolium repens), perennial
ryegrass (Lolium perenne) and plantain (Plantago lanceolata), were subjected to the following defoliation treatments: no defoliation of any

species (control) and selective trimming of all possible one-, two- and three-way combinations of the species either to 27 cm height (weak
defoliation) or to 15 cm height (strong defoliation) above the soil surface three times over a 10-week period. Successive defoliations removed
the largest amounts of shoot mass from systems in which T. repens was included among the defoliated species because T. repens dominated
aboveground plant biomass. At the ®nal harvest shoot mass was lowest in treatments that included defoliation of T. repens, while total root
mass was on average lower in strongly than in weakly defoliated systems and did not differ between the control and defoliation treatments.
Total shoot production was not affected by defoliation. Microbial basal respiration and soil NO3-N concentration differed between the
combinations of defoliated species; e.g. microbial respiration was on average 32% lower in systems in which only L. perenne was defoliated
than in systems in which only T. repens was defoliated. Microbial biomass and soil NH4 ±N concentration were not signi®cantly affected by
defoliation treatments. Enchytraeid abundance differed signi®cantly between the combinations of defoliated species: in systems in which
only L. perenne was defoliated enchytraeid abundance was on average 88% lower than in systems in which all species or only T. repens were
defoliated. Enchytraeid abundance was also positively associated with total defoliated shoot mass. Abundances of both bacterial-feeding and
fungal-feeding nematodes were affected by the combination of defoliated species; e.g. the abundance of bacterial feeders was on average
52% lower in systems in which only T. repens was defoliated than in systems in which both P. lanceolata and T. repens were defoliated.
Fungal-feeding nematodes were also more numerous in strongly than in weakly defoliated systems and positively associated with total
defoliated shoot mass. Herbivorous nematode abundance was not signi®cantly affected by defoliation treatments. The results show that the
response of soil food webs to defoliation can be affected by which combination of species in a plant community is defoliated. Further, it
seems that the role of the combination of species that are defoliated may for some components of the soil biota (e.g. fungal-feeding
nematodes) be explicable simply in terms of the total mass of foliage removed. However, for other components of the soil biota (e.g.
bacterial-feeding nematodes and enchytraeids) species-speci®c properties of different plant species in the combination of defoliated species
are also clearly important, over and above simple mass removal effects of defoliation. q 2001 Elsevier Science Ltd. All rights reserved.

Keywords: Decomposers; Defoliation; Grassland; Mini-ecosystem; Soil food web

1. Introduction
It is becoming increasingly appreciated that aboveground
herbivory may substantially in¯uence the structure of
belowground food webs and that soil food-web responses
* Corresponding author. Present address: Department of Biological and
Environmental Science, University of JyvaÈskylaÈ, P.O.Box 35 (YAC),
FIN-40351 JyvaÈskylaÈ, Finland. Tel.: 1358-14-2604199;
fax: 1358-14-2602321.
E-mail address: jmikola@jyu.® (J. Mikola).

need to be known in order to better understand the role of
herbivory in determining community and ecosystem-level
properties (Bardgett et al., 1998). One of the main processes
linking aboveground grazers and soil systems is defoliation
of plants, which is known to alter the proportion of
resources that plants allocate to root growth and exudation
(Bentley and Whittaker, 1979; Detling et al., 1979;
Richards, 1984; Miller and Rose, 1992; Holland et al.,

1996), which in turn is likely to affect nutrient uptake by
plants (McNaughton and Chapin, 1985; Ruess, 1988).
However, few experimental studies have investigated how

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PII: S 0038-071 7(00)00131-0

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J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

defoliated species, and whether the combination of the
species which are defoliated is able to in¯uence the effect
of defoliation intensity on belowground systems.

2. Materials and methods

Fig. 1. Monthly means of daily minimum and maximum outdoor temperatures and photoperiod length during the experiment.

defoliation effects are propagated through soil food webs

and those that have do not show consistent trends. The
response of the soil microbial biomass to defoliation is
positive in some studies (Holland, 1995; Mawdsley and
Bardgett, 1997) and neutral in others (Wardle and Barker,
1997). Similarly, defoliation has been shown to have both
positive and negative effects on the components of soil
fauna (Stanton, 1983; Ingham and Detling, 1984; Seastedt
et al., 1988).
Plant species differ in their resource allocation to shoot
and root growth when defoliated (Bentley and Whittaker,
1979; Richards, 1984; Wilsey et al., 1997), and in their
ability to sustain microbes and microbial-feeding nematodes
in their rhizospheres (Grif®ths, 1990; Grif®ths et al., 1992;
Wardle and Nicholson, 1996). Further, Mawdsley and
Bardgett (1997) have shown that the magnitude of the
response of soil microbes to defoliation may depend on
the plant species defoliated. It is therefore reasonable to
expect that the effect of defoliation on soil food webs in a
multi-species plant community depends on which species, or
combination of species, in the community is preferentially

consumed and thus suffers the greatest defoliation.
To better understand the effects of defoliation on soil food
webs in grasslands, and especially differential effects of
defoliation of different plant species in the grassland
community, we established a greenhouse experiment
based on replicated grassland systems composed of
mixtures of three plant species Ð white clover (Trifolium
repens L.), perennial ryegrass (Lolium perenne L.), and
plantain (Plantago lanceolata L.). We defoliated different
combinations of these species at two intensities with the aim
of testing the extent to which the effect of defoliation on soil
food-web structure depends on the combination of

We performed a greenhouse experiment based on 90
experimental units; each unit consisted of a plant community established in a white plastic container (height 32 cm,
bottom 21 £ 21 cm; drainage holes in the bottom). Soil
(with a C content of 4.7%, a N content of 0.4%, and a pH
of 6.0) was collected from a cropping ®eld at Lincoln, New
Zealand, in late June 1998, passed through a 6-mm sieve,
thoroughly mixed, and 2.20 kg (dry weight) added to each

container (forming a 5 cm deep layer). No organisms were
removed from or added to the soil prior to the experiment. In
the greenhouse lighting was not controlled but followed
natural photoperiod length (see Fig. 1). During winter
months temperature was maintained above 108C, and in
summer ventilation and fans were used to maintain temperature close to outdoor values (see Fig. 1). Containers were
placed on metal trays, and irrigated periodically by ®lling
the trays with water.
For establishing plant communities, we chose three
common grassland species and of these cultivars that have
a relatively upright growth habit and a positive response to
defoliation; i.e. white clover (Trifolium repens L. cv
Grasslands Kopu), perennial ryegrass (Lolium perenne
L. cv Grasslands Nui) and plantain (Plantago lanceolata
L. cv Ceres Tonic) (see Barker et al. 1993; Hay and Newton
1996; Stewart, 1996). Plants were raised from seeds sown
into vermiculite in plastic propagation trays, and at the age
of nine weeks (beginning of week 1 in the experiment, mid
July 1998) two seedlings of each species were planted into
each container. These plants were allowed to grow for

further 22 weeks before imposing the treatments. Containers were weeded twice to remove unwanted plants, and
before imposing the actual treatments plants were trimmed
twice; at week 18 L. perenne and P. lanceolata were
trimmed to15 cm above the soil surface to reduce competitive suppression of T. repens, and at week 28 all species
were trimmed to 27 cm above the soil surface. Plants were
regularly checked for fungal attack throughout the experiment, and spray applications of the fungicides triforine (as
Saprol) and chlorothalonil 1 thiophanate (Taratek 5F) were
made to plants in each container at weeks 12, 18, 19 and 37.
Similarly, the insecticide pirimicarb (Pirimor 50) was
applied as a spray to plants in each container at weeks 18,
37 and 39 in response to observed aphid infestations in the
greenhouse.
Defoliation treatments were started at week 32 (mid
December 1998): 15 treatments were set up at this time,
i.e. a non-defoliated control and a factorial design of
seven species defoliation treatments £ two trimming
heights. The species defoliation treatments consisted of

J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

Fig. 2. Total defoliated shoot mass (mean 1 1 SE; n ˆ 6† in relation to
defoliation treatments in a three-species grassland system. White and
hatched bars represent systems that were defoliated 27 and 15 cm above
soil surface, respectively, P ˆ Plantago lanceolata defoliated, L ˆ Lolium
perenne defoliated, T ˆ Trifolium repens defoliated, PL ˆ both P. lanceolata and L. perenne defoliated, etc.

207

trimming of each of the three species singly in the sward as
well as all the possible two- and three-way species combinations, while the trimming heights were either 27 cm (later
referred to as weak defoliation) or 15 cm (strong defoliation) above the soil surface. The combinations of defoliated
species are subsequently referred to using the following
letters: P for Plantago, L for Lolium and T for Trifolium
(see Figs. 2±6). These defoliation treatments were imposed
on the grassland community three times Ð at weeks 32, 36
and 40. Each treatment was replicated six times and the
experiment arranged in a replicate block design; each of
the six replicate blocks was positioned on a separate
irrigation tray throughout the experiment. All live plant
material cut from the defoliated plants was sorted into

species, dried and weighed. Plant parts, such as leaves
and ¯ower stems, were not separately weighed, and
trimmed material was collectively referred to as shoot

Fig. 3. Plant properties (mean 1 1 SE; n ˆ 6† in relation to defoliation treatments in a three-species grassland system at ®nal harvest. White and hatched bars
represent systems that were defoliated 27 and 15 cm above soil surface, respectively, C ˆ control (no species defoliated), P ˆ Plantago lanceolata defoliated,
L ˆ Lolium perenne defoliated, T ˆ Trifolium repens defoliated, PL ˆ both P. lanceolata and L. perenne defoliated, etc., # ˆ mean differs from the control
mean at P , 0:10; * ˆ mean differs from the control mean at P , 0:05:

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J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

Fig. 4. Shoot production (mean 1 1 SE; n ˆ 6†; consisting of both defoliated and harvested shoot material, in a three-species grassland system. Treatment
labels and statistical symbols are as for Fig. 3.

mass. At each of the three defoliation events, dead plant
tissue was removed from the containers to reduce potential fungal growth on plants. Consequently, all shoot
mass and production data of plants are based on live

shoot mass collected at each of the three defoliation
events and at the ®nal harvest.
Each container was destructively harvested at week 42
(late February 1999), two weeks after the ®nal defoliation

Fig. 5. Microbial properties and inorganic N (mean 1 1 SE; n ˆ 6† in relation to defoliation treatments in soil of a three-species grassland system at ®nal
harvest. BR ˆ basal microbial respiration, SIR ˆ substrate induced microbial respiration, treatment labels and statistical symbols are as for Fig. 3.

J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

Fig. 6. Abundance of: (a) enchytraeids; (b) rotifers (mean 1 1 SE; n ˆ 6† in
relation to defoliation treatments in soil of a three-species grassland system
at ®nal harvest. Treatment labels and statistical symbols are as for Fig. 3.

was performed. All aboveground biomass was ®rst
removed, sorted into species, dried and weighed. To estimate root mass, four subsamples of soil (totalling 430 g dry
weight (d.w.) equivalent) were taken from each container;
the roots were then extracted by washing, dried and
weighed. Of soil fauna we determined the abundance of
micro- and mesofauna; they were extracted from six

subsamples of soil (totalling 110 g d.w.) using a variant of
the tray method described by Yeates (1978). Total nematodes, enchytraeids and rotifers were ®rst counted live at
40 £ magni®cation before ®xing the suspension by the
addition of an equal volume of boiling 8% formaldehyde.
Subsequently an average of 120 nematodes per sample were
identi®ed to nominal genus, typically using 400 £ magni®cation, and allocated to trophic groups according to Yeates
et al. (1993). Finally, for microbial and inorganic N
measurements, six subsamples of soil (totalling 270 g
d.w.) were taken from each container and passed through a
4-mm mesh sieve prior to analysis. KCl-extractable NH4-N
and NO3-N concentrations of the soil were determined using
Technicon Autoanalysis. Microbial basal respiration and
substrate-induced respiration (SIR, a relative measure of
active microbial biomass) were determined as described
by Wardle (1993), based on the approach by Anderson
and Domsch (1978). Brie¯y, a 7.4 g (dry weight basis)
subsample of sieved soil, with a moisture content adjusted
to 35% (d. w. basis) was placed in a 169-ml sealed container
and incubated at 228C. Basal respiration was determined as
the total CO2-C released between one and four hours of

209

incubation, measured using infra-red gas analysis. SIR
was measured in the same way, except that samples were
amended with 10 mg glucose per g soil (wet weight)
immediately prior to incubation.
Results were statistically analysed using the SPSS statistical package (SPSS, 1999). To determine which of the 14
different defoliation treatments produced effects that
differed signi®cantly from the non-defoliated control, each
of the treatments was compared against the control using
Dunnett's test. Effects of the combination of defoliated
species and defoliation intensity were further tested using
a two-way Analysis of Variance (ANOVA; control was
excluded from these tests). After ANOVA, differences
between the means of the seven combinations of species
defoliations were tested using the Student±Newman±
Keuls (SNK) test at the signi®cance level of P ˆ 0:05 If
the effect of the combination of defoliated species was
statistically signi®cant, we used a regression analysis to
determine whether total variation across experimental
units for the dependent variable was signi®cantly explained
by total defoliated shoot mass. Homogeneity of variances
was checked using Levene's test (Dunnett's test and
ANOVA) and residual plots (regression analysis), and to
satisfy the assumption of homogeneity of variance, a logarithmic or a square-root transformation was applied to
dependent variables whenever necessary.

3. Results
3.1. Plant properties
Trifolium repens dominated aboveground plant biomass
and consequently defoliation removed the largest amounts
of shoot mass from the systems in which T. repens was
included among the defoliated species (Fig. 2). Relative to
the control, shoot mass at the ®nal harvest was lower in
those defoliation treatments, which included T. repens
(Fig. 3a), and was on average higher in the weakly than in
the strongly defoliated systems (Fig. 3a; Table 1). Shoot
mass of T. repens was lower when defoliated than in the
control and was not affected by defoliation of L. perenne or
P. lanceolata (Fig. 3b). Plantago lanceolata shoot mass was
signi®cantly lower in the strongly defoliated P and PL
treatments than in the control, and was also affected by
the defoliation of other species: harvested P. lanceolata
shoot mass was higher in the strongly defoliated T and LT
treatments and marginally higher …P , 0:10† in the weakly
defoliated L treatment than in the control (Fig. 3c). Lolium
perenne shoot mass was lower in the strongly defoliated L,
PL and LT treatments than in the control (Fig. 3d). Total
root mass did not differ between the control and defoliation
treatments (Fig. 3e), but was on average lower in strongly
than in weakly defoliated systems (Fig. 3e; Table 1). Root
mass appeared to be lower in systems where T. repens was
defoliated than in those systems where it was not, although

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J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

Table 1
ANOVA of the effects of the combination of defoliated species and defoliation intensity on plant and soil food-web properties (non-defoliated control excluded
from analyses)
Source of variation

Dependent variable

Plant properties
Total shoot mass
Total shoot production
Total root mass

Combination of
defoliated species
F6,70 a
P

Signi®cant differences
between combinations
(according to SNK-test)
Defoliation intensity

Combination £ Intensity

F1, 70

P

F6, 70

P

27.88
1.41
2.42

, 0.001
0.221
0.035

54.11
2.35
7.83

, 0.001
0.130
0.007

2.46
0.57
0.82

0.032
0.751
0.560

T, PT, LT, PLT , P, L, PL b

2.67
0.45
4.03
1.34

0.022
0.844
0.002
0.252

0.02
2.04
3.04
0.93

0.880
0.158
0.086
0.338

0.93
0.87
0.55
0.41

0.480
0.520
0.771
0.869

L,T

Abundance of enchytraeids and rotifers
Enchytraeids
3.53
Rotifers
1.25

0.004
0.292

1.74
1.11

0.191
0.296

0.71
0.81

0.639
0.563

P, L , T, PLT

Abundance of nematode trophic groups
Bacterivores
2.39
Fungivores
3.57
Fungivores to bacterivores ratio
1.44
Herbivores/unit soil mass
0.36
Herbivores/unit root mass
0.62

0.037
0.004
0.212
0.903
0.718

0.61
4.76
1.95
2.41
, 0.01

0.437
0.032
0.167
0.125
0.999

1.58
0.53
0.61
0.46
0.67

0.165
0.787
0.720
0.835
0.675

T , PT
PLT . others

Soil microbes and inorganic N
Basal microbial respiration
Substrate induced respiration
NO3-N concentration in soil
NH4-N concentration in soil

a
b

T , P, PL, PLT

Degrees of freedom of treatment and error.
P ˆ Plantago lanceolata defoliated, L ˆ Lolium perenne defoliated, T ˆ Trifolium repens defoliated, PL ˆ both P. lanceolata and L. perenne defoliated,

etc.

the SNK-test could not locate signi®cant differences
between treatment means (Fig. 3e, Table 1). Root mass
was negatively associated with total defoliated shoot mass
(regression analysis: R2 ˆ 0:158; P , 0:001†:
Total shoot production did not differ between the control
and defoliation treatments (Fig. 4a), and was not affected by
the combination of defoliated species or by defoliation
intensity (Fig. 4a; Table 1). Similarly, no differences were
found between the control and defoliation treatments with
regard to the shoot production of T. repens and L. perenne,
whereas the shoot production of P. lanceolata was signi®cantly higher in the strongly defoliated LT and PLT treatments than in the control and marginally higher …P , 0:10†
in the strongly defoliated T treatment (Fig. 4b±d).
3.2. Soil microbial properties and inorganic N
No statistically signi®cant differences were found
between the control and the defoliation treatments with
regard to soil microbial properties or concentrations of inorganic N in soil, except that basal respiration was marginally
higher …P , 0:10† in the intensely defoliated T treatment
than in the control (Fig. 5). However, there were statistically
signi®cant differences between the combinations of defoliated species with regard to basal respiration and NO3-N
concentration: basal respiration was on average lower in the

L treatment than in the T treatment, and NO3-N concentration was lower in the T treatment than in the P, PL and PLT
treatments (Fig. 5a and d, Table 1). Neither basal respiration
nor soil NO3-N concentration were signi®cantly affected by
total defoliated shoot mass (regression analyses: R2 ˆ 0:02;
P ˆ 0:272 and R2 ˆ 0:027; P ˆ 0:135; respectively).
3.3. Soil fauna
Enchytraeid abundance was signi®cantly higher in
the intensely defoliated T and PLT treatments than in the
control (Fig. 6a), and on average higher in the T and PLT
treatments than in the P and L treatments (Fig. 6a, Table 1).
Enchytraeid abundance was also positively associated
with total defoliated shoot mass (regression analysis:
R2 ˆ 0:157; P , 0:001†: Rotifer abundance did not differ
between control and defoliation treatments (Fig. 6b) and
was not signi®cantly affected by the combination of
defoliated species or defoliation intensity (Fig. 6b, Table 1).
No statistically signi®cant differences between the
control and the defoliation treatments were detected with
regard to the abundance of nematode trophic groups, except
that higher fungivore abundance was detected in the
strongly defoliated PLT treatment than in the control
(Fig. 7). Further, the ratio of abundance of fungal-feeding
nematodes to that of bacterial-feeding nematodes did not

J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

211

Fig. 7. Abundance of nematode trophic groups, and ratio of abundance of fungal-feeding to bacterial-feeding nematodes (mean 1 1 SE; n ˆ 6† in relation to
defoliation treatments in soil of a three-species grassland system at ®nal harvest. Treatment labels and statistical symbols are as for Fig. 3.

differ between the control and the defoliation treatments
(Fig. 7c). Abundances of both bacterivores and fungivores
were, however, affected by the combination of defoliated
species and defoliation intensity: bacterivores were on average more numerous in the PT treatment than in the T
treatment (Fig. 7a, Table 1), and fungivores were more
numerous in strongly than in weakly defoliated systems
and more abundant in the PLT treatment than in the other
combinations of defoliated species (Fig. 7b, Table 1).
Variance in bacterial-feeding nematode abundance was
not explained by total defoliated shoot mass (regression
analysis: R2 ˆ 0:025; P ˆ 0:153†; whereas the abundance
of fungal-feeding nematodes and total defoliated shoot
mass were positively associated (regression analysis:
R2 ˆ 0:105; P ˆ 0:003†: Herbivorous nematode abundance,
either per unit root mass or per unit soil mass, and the
ratio of fungivore abundance to bacterivore abundance
were not statistically signi®cantly affected by the

combination of defoliated species or defoliation intensity
(Fig. 7c±e; Table 1).

4. Discussion
Our results show that the response of soil food webs to
defoliation can be affected by which combination of species
in a plant community is defoliated. In our case, the combination of defoliated species appeared to have more in¯uence
on the soil food web than did defoliation intensity, but it did
not appear to modify the effect of defoliation intensity. Total
defoliated shoot mass was not equal in the different
combinations of defoliated species, and in many cases
when a dependent variable was signi®cantly affected by
the combination of defoliated species, variance in the
dependent variable was also signi®cantly explained by
total defoliated shoot mass. This means that the signi®cant

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J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

effect of the combination of defoliated species on some soil
variables may be explicable in terms of total defoliated
shoot mass.
Although shoot mass at harvest differed across defoliation
treatments, defoliation did not affect total shoot production,
a pattern which appears to be common for grassland species
(Wilsey et al., 1997). Since root mass was on average lower
in strongly than in weakly defoliated systems, plants
increased allocation of resources to shoot growth when
defoliation intensi®ed. Higher allocation to shoot than root
growth after defoliation has been observed in several studies
(Detling et al., 1979; Richards, 1984; Ruess, 1988; Polley
and Detling, 1989; but see Milchunas and Lauenroth, 1993),
and it appears to be typical for species that are adapted to
intense but infrequent defoliation (Wilsey et al., 1997). Our
results also show that the three plant species differed in their
response to defoliation and that the response was partly
determined by the level of the dominance of the species in
the community. The least dominant species, P. lanceolata,
bene®ted signi®cantly from the defoliation of the other
species, which is apparent through the high shoot production
of P. lanceolata even in systems where it, in combination
with the other species, was subjected to defoliation. In
contrast, T. repens was only affected by direct defoliation
and did not bene®t through the defoliation of other species.
The overall activity and biomass of soil microbes were
little affected by defoliation in our experiment; the only
response to treatments was the lower basal respiration in
the L treatment than in the T treatment. It has been
suggested that increased root exudation and root mortality
of defoliated plants could lead to the increased microbial
activity and biomass observed in the rhizosphere of
defoliated plants (Holland, 1995; Holland et al., 1996;
Mawdsley and Bardgett, 1997). This would suggest that
microbes were more active in the T treatment than in the
L treatment because the greater amount of foliage that was
removed from the T treatment induced higher root
exudation and mortality in these systems. However, basal
respiration was generally not signi®cantly affected by total
defoliated shoot mass, which suggests that some speciesspeci®c property other than simply the amount of defoliated
shoot mass determined microbial activity in our experiment.
While on average more NO3-N tended to be available in
strongly than in weakly defoliated systems, less NO3-N
was found in the T treatment than in the P and PL treatments
and total defoliated shoot mass did not signi®cantly affect
NO3-N concentration in soil. This suggests that the concentration of inorganic N in soil is not necessarily purely
determined by total defoliated shoot mass but also depends
on other species-speci®c properties of the defoliated
species.
Highest abundances of microbi-detritivorous enchytraeids were found in the T and PLT treatments, in which
defoliation removed large amounts of shoot mass. As
enchytraeid abundance was also positively associated with
total defoliated shoot mass, defoliation in general appeared

to increase enchytraeid abundance in soil, possibly through
higher root mortality in strongly defoliated systems.
However, since enchytraeid abundance in the PT and LT
treatments did not signi®cantly differ from that in the P, L
and PL treatments, the response of enchytraeids to defoliation cannot solely be explained in terms of the net amount of
plant mass removed, but other effects of the composition of
defoliated species also appear to be important.
Bacterial-feeding faunae were in general only slightly
affected by the treatments; no effects were detected for rotifers and the only signi®cant effect for the bacterial-feeding
nematodes was their lower abundance in the T treatment
than in the PT treatment. Only one previous study exists
in which the effects of arti®cial defoliation on soil bacterial-feeding faunae have been investigated; in that a negative
response of bacterial-feeding nematodes to defoliation was
found (Stanton, 1983). Our results suggest that the effect of
defoliation on bacterial-feeding nematodes may depend on
the plant species defoliated. In contrast to bacterial feeders,
fungal-feeding nematodes clearly responded to defoliation
in our study; they were more numerous in intensely than
weakly defoliated systems, more abundant in the PLT treatment than in the other defoliation combinations, and also
positively associated with total defoliated shoot mass. This
shows that defoliation in general enhanced fungivore abundance in soil, possibly through higher root mortality and the
subsequent enhanced growth of fungi. Some ®eld studies
have shown that the ratio of fungi to bacteria (Bardgett et
al., 1996; 1997) and the ratio of fungal-feeding nematodes to
all soil nematodes (Freckman et al., 1979; Wall-Freckman
and Huang, 1998) tend to be higher in grazed than in
ungrazed grasslands, which implies that grazing may
cause a shift between the bacterial-based and the fungalbased energy channels (see Moore and Hunt, 1988). In our
experiment the ratio of fungivorous to bacterivorous nematodes was not affected by defoliation treatments, which
implies that defoliation per se may not cause a shift between
the two energy channels.
In contrast to previous studies, in which defoliation and
animal grazing have often been shown to increase abundances of soil herbivores either per unit soil or root mass
(Smolik and Dodd, 1983; Stanton, 1983; Ingham and
Detling, 1984; Yeates, 1976; Seastedt et al., 1988; Merrill
et al., 1994; but see Leetham and Milchunas, 1985; WallFreckman and Huang, 1998), total abundance of herbivorous nematodes was not statistically signi®cantly affected by
defoliation in our study. It may therefore be that intense
defoliation of all species of the plant community is needed
to produce signi®cant changes in the abundance of rootfeeders.
The total quantity of shoot mass removed by defoliation
and species-speci®c traits independent of mass removal by
defoliation are both likely to have important effects on the
belowground subsystem in our study. Responses of some
soil variables infer that the combination of defoliated
species had a role in determining the response of the

J. Mikola et al. / Soil Biology & Biochemistry 33 (2001) 205±214

belowground system independently of the mass of material
that was defoliated; for example, microbial activity, inorganic N and abundance of bacterial-feeding nematodes were
all affected by the combination of defoliated species but not
by total defoliated shoot mass. In contrast, the response of
fungal-feeding nematode abundance to the defoliation of
different species combinations appeared to be mostly
explained by its response to the total amount of plant
biomass removed by defoliation. Enchytraeid abundance
appeared to be affected by both total defoliated mass and
by species combination effects over and above this. Effects
of species combinations on community and ecosystem
response variables have usually been found to be idiosyncratic and dif®cult to predict based on the effects of single
species; studies which have involved mixing litter from
different plant species (Blair et al., 1990; Wardle et al.,
1997; Nilsson et al., 1999), combining soil faunal species
(Faber and Verhoef, 1991; Mikola and SetaÈlaÈ, 1998), and
growing plant species in mixtures (Wardle and Nicholson,
1996) have all proved to have idiosyncratic effects on soil
variables. Whether defoliating different combinations of
plant species will also bring about idiosyncratic responses
in the belowground system over and above the effects of
mass of foliage removed, as our study suggests, needs to be
further tested in communities in which shoot mass is more
evenly distributed across species.
Acknowledgements
This work was supported by a grant from the New
Zealand Marsden fund to D.A.W. and G.M.B.
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