Decomposition and Nitrogen Mineralization in Natural and Agroecosystems - the Contribution of Soil Animals

Abstract

The present article centres on the contribution of soil animals to organic. matter decomposition and nitrogen mineralization
in natural and agro-ecosystems. Criteria are presented for the categorisation of the soil fauna in functional groups in order
to be able to quantify the contribution of the soil fauna. Three types of classifications: size, habitat and food, are discussed.
For various natural ecosystems, such as prairies and forests, and for agro-ecosystems a rather similar outcome of the faunal
contribution to nitrogen mobilization of approximately 30% appears to exist. This value is dependent on various types of interactions
among functional groups, changes in population density of microorganisms and soil fauna, seasonally changing abiotic factors
and management, such as fertilization, harvesting and addition of harvest residues to the soil. Finally, to improve management
of ecosystems as related to soil faunal activity in decomposition, lines are set out for further research such as the development
of dynamic models, studies concerning the effects of perturbation in relation to microbial dominance and the integration of
the study of below-ground food webs with ecological theories.

Full text

Biogeochemistry
11:
175-211,
1990
c
Kluwer
Academic
Publishers.
Printed
in
the
Netherlands
Decomposition
and
nitrogen
mineralization
in
natural
and
agro-
ecosystems:
the
contribution
of
soil
animals
H.A.
VERHOEF'
&
L.
BRUSSAARD
2
IDepartment
of
Ecology
and
Ecotoxicology,
Free
University, De
Boelelaan
1087,
1081
HV
Amsterdam,
The
Netherlands;
2
Department
of
Soil
Biology,
Institute
for
Soil
Fertility
Research,
P.O.
Box
30003,
9750
RA
Haren,
The
Netherlands,
and
Department
of
Soil
Science
and
Geology,
Agricultural
University,
P.O.
Box
37,
6700
AA
Wageningen,
The
Netherlands
Received
28
November
1989;
accepted
12
April
1990
Key words:
Agro-ecosystems,
decomposition, management,
mineralization,
natural
ecosystems,
soil
fauna.
Abstract.
The
present
article
centres
on the
contribution
of
soil
animals
to
organic
matter
decom-
position
and
nitrogen
mineralization
in
natural
and
agro-ecosystems.
Criteria
are
presented
for
the
categorisation
of
the
soil
fauna
in
functional
groups
in
order to
be
able to
quantify
the
contribution
of
the
soil
fauna.
Three
types
of
classifications:
size,
habitat
and
food,
are
discussed.
For
various
natural
ecosystems,
such
as
prairies
and
forests,
and
for
agro-ecosystems
a
rather
similar
outcome
of
the
faunal
contribution
to nitrogen
mobilization
of
approximately
30%
appears
to
exist.
This
value
is
dependent
on
various
types
of
interactions
among
functional
groups,
changes
in
population
density
of
microorganisms
and
soil
fauna,
seasonally changing
abiotic factors and management,
such
as
fertilization, harvesting
and
addition
of
harvest
residues to
the
soil.
Finally,
to
improve
management
of
ecosystems
as
related
to
soil
faunal activity
in
decomposition,
lines
are
set
out
for
further
research
such as
the
development
of
dynamic
models, studies
concerning the
effects
of
perturbation
in
relation
to
microbial dominance and the
integration
of
the
study
of
below-ground
food
webs
with
ecological
theories.
1.
Introduction
In functional
soil
zoology studies there
appears
to
be
a
dichotomy
in
approach.
In one
approach
emphasis
is
laid
on
the processes
of
decomposition
and
nutrient
mobilization
and
the
animals
are
considered
as
one
variable.
In the
second
approach
a
complete
description
of
the
diversity
of
the
decomposer
species,
their
distribution,
abundance and
activity
is
aimed
at,
while
the proces-
ses
of
decomposition
and
mobilization
fade
into
the
background
(cf.
Usher
et
al.
1982).
In
the
first
approach
soil
animals
are
considered mainly
as
favouring
the
microbial
processes
indirectly
by
changing the
structural,
physical
and
chemical
properties
of
the
soil.
Models for
nitrogen mineralization
from
leaf
litter
have been
developed
in
which
the
effects
of
the
soil
animals
were
expressed
proportionally
to their
total
biomass
(Anderson
et
al.
1985;
Seastedt
1984).
These
models
are
useful
for describing
decomposition
as
a
process,
yet
give
little
Communication No
13
of
the
Dutch
Programme
on
Soil
Ecology
of
Arable
Farming
Systems.

176
insight
in
how
the
process
is
regulated.
Such
insight
is
needed
for
the
manipula-
tion
of
decomposition
towards
higher
use
efficiency
of
nutrients
in
man-
managed
ecosystems,
such
as
managed
forests
and
agricultural
land.
Although
the
second
approach
in
principle
can
contribute
to
obtain
the
necessary
insight,
it
is
too
laborious
to
be
practical,
unless
the
diversity
of
species
to
be
studied
is
reduced
by
lumping
them
in
functional
groups.
In
the
present
article
we
will
give
criteria
for
the
categorisation
of
the
soil
fauna
in
groups
with
more
or
less
similar
functions
in
decomposition,
in
order
to
be
able
to quantify
the
contribution
of
the
soil
fauna
to
organic
matter
degradation.
We
will
focus
on
the
contribution
of
the micro-
and
mesofauna
to
nitrogen mineralization.
After
presenting
the different
ways
of
functional
classification (section
2)
we
will
give
results
from
different
natural
ecosystems,
such
as
prairies
and
forests
and
from
agro-ecosystems
(section
3).
Following
a
discussion
of
intrinsic
in-
teractions
among
functional
groups
(section
4)
and
the
effects
of
abiotic factors
on
animal-mediated decomposition
and
mineralization
(section
5),
the
effects
of
various
perturbations
on
the
contribution
of
soil
fauna
to
element
turnover
will
be
discussed (section
6).
Finally,
we
set
out
some
lines
for
further
research,
inspired
by
the obvious
need
for
integration
of
the
studies
of
below-ground food
webs
with
ecological
theories
to
improve
management
of
ecosystems
as
related
to
soil
faunal
activity
in
decomposition
(section
7).
2.
Functional
classification
The
clear
differences,
both
qualitative
and quantitative,
between different
soil
animals
in
their
effects
on
nutrient
mineralization,
have
led
to
their
classification
into
functional groups.
These are
groups
of
organisms,
which have, irrespective
of
their taxonomical
origin,
a
similar
function
in
the process
of
mineralization
(Moore
et
al.
1988).
For
a
critical
review
of
the
functional
group
concept
see
Hawkins
&
MacMahon
(1989).
Size
classification
An often
used classification
is
that
based
on
body
width
of
the
animals,
since
this
should
broadly
reflect
the
scales
at
which
they
affect
or
effect
soil
processes:
micro-,
meso-
and
macrofauna
(Fig.
1).
Microfauna
(body width
2pm-100lm)
comprises
nematodes
and protozoa
and other
less
common
groups.
They
live
in
water-filled
pores
and
water
films
in
the
soil
matrix,
and
represent
a
diverse
assemblage
of
trophic groups,
with
fungal-,
bacterial-
and
plant-feeding
species
as
most
abundant.
Mesofauna
(100#pm-2mm)
comprises,
among
other
groups,
collembola,
mites
and
enchytraeids.
These
animals
are
largely
found
in air-filled
pores.
This
group,
too,
is
a
mixture
of
species
with
various
trophic
relationships.
Macrofauna
(2mm-20mm)
comprises,
among
others,
millipedes,
woodlice,

177
Microfauna
Mesofauna
Macrofauna
1001um
2
mm
20
mm
Nematoda
I
Protozoa I
I
Acari
Collembola
I
I
Enchytraeidae
I
Isoptera
Isopoda
I
Amphipoda
I
Diplopoda
I
Megadrili
(earthworms)
Coleoptera
I
Mollusca
I ] I I I I I I [ I I I I I
I
1
2
4
8
16
32 64
128
256
512
1024
2
4
8
16
32
64
I
I
,.im
mm
Body
width
Fig.
1.
Size-type
classification
of
soil
animals.
(After
Swift
et al.
1979)
fly
larvae,
beetles, snails
and
earthworms.
They have
body
sizes
large
enough
to
disrupt
the physical
structure
of
the
soil
through
their
feeding
and/or
burrowing
activities, as
e.g.
has
been
shown
for
lumbricid
earthworms, introduced into
pastures
(Hoogerkamp
et
al.
1983)
and
also
for
dung
beetles
(Brussaard
&
Hijdra
1986,
Fig.
2).
This
group,
too,
shows
an
assemblage
of
trophic
relationships.
Habitat
classification
A
second
functional
classification
is
based on
the
depth
in
the
soil
profile,
at
which
the
animals
live.
Earthworms
can
be
classified
into
epigeal
(surface-
active)
species,
which
are
largely
involved
in
litter
comminution;
endogeic
species,
which are
geophagous
and
live
in
the
mineral
soil;
and
anecic
species
which
transport
materials
between
mineral
soil
and
the
organic
litter
layer
(Bouch&
1977;
Springett
1983).
Such
a
stratified
distribution
has
also been
found
for
several
linyphiid
spiders
(Kessler
&
van der
Ham
1988).
In
soils
with pore
sizes
diminishing downwards,
there
is
an overlap
between
size
and
habitat
classification.
A
similar
classification
has
been
proposed
for
collembola (Verhoef
1986).
In

178
30
20
E
10
45-60
50-55 50-55
80-85
90-105
cm
below
surface
Fig.
2.
Effect
of
back-filling
burrows
by
dung
beetles
on
soil
macroporosity.
Blank
bars:
undisturbed
soil
matrix;
hatched
bars:
dung
beetle
burrows,
back-filled
to
a
lower
bulk
density
than
the original
soil
matrix.
(From
Brussaard
&
Hijdra
1986)
this
group
a
distinction
can
be
made
between
epigeic,
hemiedaphic
and
eue-
daphic
representatives
(Fig.
3),
originally based
on morphological
differences
(Gisin
1943).
Great
differences
between,
and
similarities
within
the
three
catego-
ries
have
been
found
concerning their
ecophysiology
(Verhoef
1978;
Testerink
1981;
Witteveen
1986;
van
der
Woude
1988;
Joosse &
Verhoef
1987)
and
their
population
biology
(van
Straalen
1983;
Vegter
1985).
These
properties
have
been
summarized for
the
epigeic
and
the euedaphic category
in
Table
1.
The
hemiedaphic
group
is
intermediate.
In
addition,
there
is
evidence
that
epigeic
animals
play
a
role
in
the
initiation
I1
ma <~m
Fig.
3.
Distinction
in
epigeic
(I),
hemiedaphic (II)
and
euedaphic
(III)
collembola,
based
on
morphological
differences.
(From
van
Straalen
et
al.
1985)

179
Table
1.
Ecophysiological
and
population
biological
characteristics
of
epigeic
and
euedaphic
collem-
bola.
Epigeic
Euedaphic
category
Drought
tolerance
Drought
susceptibility
High
metabolic rate
Low
metabolic
rate
High
locomotory
activity
Low
locomotory
activity
Temperature
dependent
development
Temperature
independent
development
Seasonally
induced
life
cycle
Seasonally
independent
reproduction
Sexual
reproduction,
sexual
dimorphism
Parthenogenesis
Courtship
behaviour
Random
spermatophore-deposition
High
fertility,
high
mortality
Low
fertility,
low
mortality
From
van Straalen
et
al.
1985
of
decomposition,
whereas euedaphic
animals would
affect
later
stages
of
de-
composition and
have a
direct
effect
on
mineralization
processes
(Verhoef
et
al.
1988).
This
has
been
shown
for
three collembolan
species
coexisting
in
high
abundances
in
coniferous
forest
soils,
i.e.
Orchesella
cincta
(L.),
Tomocerus
minor
(Lubbock)
and
Isotoma
notabilis
(Schiffer).
These
three
species
are
epi-
geic,
hemiedaphic
and
euedaphic,
respectively.
Field experiments,
in which
presence
and
density
per
species were
manipulated,
showed
for
the
three
species
different
effects
on
decomposition
rate,
changes
in
total
nitrogen
and
leaching
of
mineral
nitrogen
(Faber
&
Verhoef
1990).
The
species
are
not
strictly segregated
vertically.
They may
migrate
up and
down
due
to
microclimatical
changes
(van
der Woude
&
Verhoef
1986).
Lab-
oratory
studies
using
microcosms
show only
in
the
F
layer
a
clear
effect
for
the
hemiedaphic Tomocerus
minor
(Verhoef
&
Dorel
1988,
Fig.
4).
So,
it
can
be
Ammonium
Leaching
(
ug
g-dm
)
100-
5o-
10'
Aoo
I~
130
-
100-
50'
1'
0 2
4
6 8
10
0
Time
(weeks)
Ao
4
6
8
10
Fig.
4.
Ammonium
leaching
from
microcosms
filled
with
L
(AOo)
and
F
layer
material
(Ao)
from
Pinus
nigra,
calculated
per
unit
mass
of
substrate,
per
two
weeks.
Go
=
with Tomocerus
minor,
o-o
=
microorganisms
only.
(From
Verhoef
&
Dorel
1988)
I
---

180
Fig.
5.
Representation
of
the
detrital
food
web in
a
shortgrass
prairie.
Fungal
feeding
mites are
separated
into
two
groups
to
distinguish
the
slow-growing
cryptostigmatids
from
faster-growing
taxa.
Flows
ommited from
the
figure
for the
sake
of
clarity
include
transfers
from
every
organism
to
the
substrate
pools (death)
and
transfers
from
every
animal
to
the
substrate
pools
(defaecation)
and to inorganic
N
(ammonification).
(From
Hunt
et
al.
1987)
concluded
that
in
a
well-stratified
soil
a
functional
classification
of
soil
animals
based
on
depth
of
occurrence
is
a
valid
one.
Food
classification
The
third
type
of
classification can
also
be
used
for
non-stratified
soils,
and
is
largely
based
on
the
trophic
relationships
of
the
different
groups
of
animals
(feeding
mode, principal
food
source).
This
classification
has
been
applied
in
a
study
in
a
shortgrass
steppe
(Hunt
et
al.
1987,
Fig.
5).
Although
functional groups
in
principle may
consist
of
animals
from
different
taxa,
ecophysiological
and
population
biological
characteristics
are usually
so
different
among
higher
taxa
that
in
practice
no
animals
from
different
orders
will
be
categorized
in
one
functional
group.
Even families
or
species
with similar
trophic
relationships
may have
to
be
placed
in
different
groups.
As
our
know-
ledge
on
feeding
behaviour
increases,
further
subdivision may
be
necessary.
Predaceous
mites
(two
functional groups
in
Hunt
et
al.
1987)
were
separated
into four groups
with
different
hunting
behaviours
and
prey
by
Walter
et
al.
(1988).
We
will
henceforth
use
food
type classifications to
quantify
the
contribution
of
soil
animals
to
decomposition and
nutrient
cycling,
with
special
emphasis
on
nitrogen.

181
3.
Quantification
of
the contribution
of
soil
animals
to
nitrogen mineralization
in
natural
and
agro-ecosystems
For
use in
decomposition
studies, the
ideal
classification
should,
above
all,
reflect
the
trophic
relationships
between
groups.
In
this
section
we
give
quantita-
tive
examples
from
a
coniferous
forest,
a
shortgrass
steppe
and arable
land.
Persson
(1983)
gave
a
food
type
classification
for
the
soil
animals
living
in
a
Pinus
sylvestris
forest
in
Central
Sweden.
In
a
nitrogen mineralization
model
estimates
were
made
with
ratios
C/N
(faeces):
C/N
(food) increasing
from
I
to
2.
Recent
budget
analyses have
shown
a
ratio
of
1.3
for collembola
(Verhoef
et
al.
1988;
unpublished
data).
Depending
on
the
choice
of
assimilation
efficiency
for nitrogen,
the
contribution
of
soil
fauna
to
total
net
nitrogen mineralization
was
estimated
to
be
between
10
and
49%.
In
a
Pinus
nigra
forest
in
The
Netherlands
the
contribution
of
soil
fauna
to
total
nitrogen
mobilization
was
approximately
30%.
This
was
calculated
with
data
from
lysimeter
studies
in
the
presence
or
absence
of
soil
animals
and/or
roots
(Verhoef
et
al.
in
prep.).The
Pinus
stand
was
on
a
fungus
dominated,
stratified
soil,
where
the
fungivorous
collembolan Tomocerus
minor
is
abundant
(mean
annual
density:
2,000
individuals
m
2).
Using
population
biological
parameters,
such
as
population
biomass,
population
turnover
rate
(van
Straalen
1985),
the
nitrogen
concentration
of
the
animal
and
its
food
and
data
on
the
individual
nitrogen budget
(Verhoef
et
al.
1988),
total
excreted
nitrogen
(both
faeces
and
urine)
amounted
to
620mg
Nm
2
y
,
which
is
170
times
their
biomass
nitrogen
per
year. This
relatively
high
nitrogen
output
is
caused
by
their
high
biomass
turnover
rate and
high
assimilation
efficiency
(see
Table
2),
causing
high
nitrogen
excretion
via
urine
(Verhoef
et
al.
1988).
In
such
stratified
coniferous forest
soils
the fungal
route
(Fig.
6)
seems
to
be
dominant.
Figure
5
concerned
the
below-ground food
web
of
the
shortgrass
steppe
of
northeastern Colorado
(USA)
(Hunt
et
al.
1987;
Moore
et
al.
1988).
The
sizes
of
the
vectors
and
compartments of
Fig.
5,
representing the nitrogen
pools
and
flows
in
this
ecosystem, are
given
in
Fig.
7.
The vector
F
represents the
flow
of
nitrogen,
mineralized
by
the
fauna.
This
is
37%
of
total
nitrogen mineralization,
even
though total
faunal
biomass
is
only
2.5%
of
that
of
saprophytic
fungi
and
bacteria.
Bacterial
feeding
amoebae
and nematodes
together
accounted for
over
83%
of
nitrogen
mineralization
by
fauna.
This
high
contribution
is
due to
the
Table
2.
Efficiencies
of
nitrogen conversion
in
Tomocerus
minor
on
an
algal*,
a
fungal**
and
a
mixed
diet***:
assimilation
efficiency
(A/C
x
100%)
and
tissue
growth
efficiency
(P/A
x
100%).
Values
are means
SE.
Diet
A/C
x
100%
P/A
x
1000/%
*
Desmococcus
70
1.5
32
2.7
**
Cladosporium
86
+
2.2
37
+
7.8
***Desmooccuws
}
78
+
2.1
29
+
3.5
Cladosm
Vrho
.
1988
From
Verhoef
et
al.
1988

182
Eat wo m
Enchytr
,ds II
Macroarhr°Pods
l M icroar
ropods
J
Fig.
6.
Conceptual
detrital
food
web
in
stratified
coniferous
forest
soils.
Boxes
=
nutrient
storages,
clouds
=
nutrient
sources
or
sinks,
and arrows
=
nutrient transfer
pathways.
Valve
symbols
on
arrows
indicate
that
nutrient
transfers
are
influenced
by
factors
connected
with
dotted
lines.
(Modified
after Hendrix
et
al.
1986)
fact
that
like
the
collembolan
T.
minor
these
groups
combine
high
turnover
rates
with
a
relatively
high
assimilation
efficiency
and
a
diet
which
is
rich
in
nitrogen.
In this
model
population
numbers
are
presented
as
average
values
over
the
growing
season.
Nitrogen
mineralization
during
the
growing
season
was
modelled
to
occur
during
40
ideal
days when the
system was
considered
in
steady
state.
Andren
et
al.
(1990)
published a nitrogen
budget
model for barley
fertilized
with
120
kg
N
ha
',
largely
based on
taxonomic groups
(Fig.
8).
Pool
sizes
of
organisms
are
mean
annual
estimates, considered
to
be
in
steady
state
and
fluxes
are
expressed
on a
per
year
basis.
They
concluded
that
in
this
system
25%
of
the
nitrogen mineralization
was
accounted for
by
the
fauna.
Here again,
protozoa
and nematodes
contributed
by
far
most to
the
nitrogen
mineralization.
Brussaard
et
al.
(in
prep.) quantified
soil,
plant
and
biota
nitrogen
in
winter
wheat
in
The
Netherlands.
The
data
on
nitrogen pools
in
various
taxonomic
groups
are
given in
Fig.
9.
As
compared
with
the
data
from
Sweden
(460kg
N
ha-',
Andren
et
al.
1990)
for barley,
fertilized
with
120
kg
N
ha
',
the
fungal

183
a
Fig.
7.
Nitrogen
flux
description
of
the
detrital
food
web.
The
sizes
of
vectors
and compartments
represent the
relative
sizes
of
nitrogen
flows
(g
N
m
2
yr-')
and
compartment
biomass
(g
N
m
2).
Vectors
and compartments
are laid
out
as in
Fig.
5.
F
represents
nitrogen
mineralization
by
fauna.
(From
Moore
et
al.
1988;
data
from
Hunt
et
al.
1987)
nitrogen
pool
was
considerably
lower
in
The
Netherlands
(3.1-4.7
kg
N
ha
-',
Fig.
9).
Pools
of
protozoa,
nematodes and enchytraeids
were
approximately half
the
sizes
of
the
pools
in
the
Swedish
soil,
while
arthropod
pools
were
similar
in
size.
No apparent
differences in
faunal biomass
were assessed
between
the
two
farming
systems
in
The
Netherlands,
to
which
the
data
refer,
during
the
first
year
of
their
existence.
Presumably,
modelling the
contribution
of
the
soil
fauna
to
nitrogen mineralization
in
the
two
systems,
will yield
a
result in
the
same
order
of
magnitude
as
in
the
above-mentioned
studies.
Perhaps
the
most
striking
feature
of
the
studies described
above
is
the
rather
uniform
outcome
of
the
faunal
contribution
to nitrogen mineralization
of
approximately
30%.
The
calculations
of
the studies
are
based,
however,
on
assumed steady
state
populations.
It
is
necessary
to
introduce
into
such
models
dynamic
factors
such
as
various
types
of
interactions,
changes
in
population
density,
seasonally
changing
abiotic
factors,
resource
quality
and
management,
e.g.
to
better
describe
and
predict
the
match
between
supply
of
nitrogen
by
the
soil
and
demand
from
the
crop.

184
Herbivores
Predators
-----
I
FA'
I
98
I
-
98
1
_ _ _
Fig.
8.
Nitrogen
food
web
of
the Kjettslinge
field,
exemplified
with
data
from
fertilized
barley
(B
120).
Values
in
the
boxes
indicate biomass
nitrogen
(mg
N
m-
2
)
at
harvest
for
the
plant; for
other
organisms
mean
values
for September
1982-1983
are
given.
On the
left side
of
each box
consump-
tion
(mg
N
m-2yr
)
is
indicated, calculated
using energetic
quotients.
All
biomass
values
are
given
for
the
top
soil,
0-27cm
depth.
Nitrogen
mineralization
is
indicated
by
values
under
each
box.
(Bacteria
=
Ba,
Protozoa
=
Pr,
Nematodes
=
Ne,
Herbage
arthropods
=
Ha,
Soil
macroarthropods
=
Sm,
Acari
=
Ac,
Collembola
=
Co,
Earthworms
=
Ea).
Nitrogen
miner-
alization
was
divided
between
bacteria
and
fungi
for
practical
reasons; only
the sum
(7000)
is
relevant.
(From
Andren et
al.
1990)
4.
Dynamic
interactions
among
functional
groups
In
quantitative
studies
of
energy
and
nutrient
transfer, mutualistic
effects
are
implicit
in
the
pool
sizes
and
flow
rates
concerning
the
prey
groups,
whereby
the
importance
of
grazing
or
predator
groups for
energy
and
nutrient
transfer
may

185
Bacteria
Fungi
Flagellates
-*
<
Amoebae
Nematodes
IMM
EMites
Collembola
Enchytraeids
-~~~~~~~~~~~~~~
0
1
2
3
4
5
Average
Npool
(log(kgNx10
)ha
1
)
Fig.
9.
Average
nitrogen pools
in
various
taxonomic groups
of
the
soil
biota
in
a
winter
wheat
growing season
in
1986
in
a
conventional
and
a
first
year's integrated cropping
system
on
a
silt
loam
soil
(pH
7.5)
in
The
Netherlands. Conventional
(black
bars):
total
soil C
2.2%;
total
N
0.09%;
inorganic N
(spring)
+
Ca(NO3)
2
-N
193
kgha
i'.
Integrated
(open
bars):
total
C
2.8%;
total
N
0.14%:
inorganic
N
(spring)
+
Ca(NO
3
)
2
-N
156kgha
i.
(From
Brussaard
et al.
in
prep.)
be
underestimated
(cf.
Hunt
et
al.
1987;
Moore
1988;
Moore
et
al.
1988).
Evidence
therefore can
be
derived
from
microcosm-studies
and
field
studies
at
increasingly
complex
interactive
levels:
Two-component
interactions
Quantification
of
the
effects
of
grazing
on microbial metabolism
gave
different
results
depending
on
the
interaction
studied
(Morley
et
al.,
cited by
Elliott
et
al.
1986).
In
a
microcosm-study
with
grassland
soil
organisms
on
the decomposi-
tion
of
purified
cellulose
in
the
presence
of
chitin
the
addition
of
the
fungus
Fusarium
oxysporum
caused
a
higher
CO
2
evolution
than
the
addition
of
the
bacterium
Flavobacterium
sp.
(Trofymow
et
al.
1983).
Grazing
by
the
fun-
givorous
nematode
Aphelenchus
avenae
did
not
increase
total
CO
2
evolution,
whereas
grazing
by
the
bacterial-feeding
nematode
Pelodera
sp.
significantly
increased
CO
2
evolution. In
both
cases
grazing
enhanced
ammonium
minerali-
zation.
In collembola-fungi
interactions
the density
of
the grazers
is
important.
These
effects
of
increasing density
of
collembola on fungal biomass
and
on nitrogen
mobilization
are
shown
in
Fig.
10
(Anderson
&
Ineson
1984).
At
the
start
of
this
microcosm-experiment
low
numbers
of
the
fungivorous
Folsomia
candida
sti-
mulated
fungal
biomass,
whereas
after
8
weeks
high
numbers
of
these
animals
i
l

186
E
28-
E
E
20-
.,
U-
;-
ZO-
39
15
c
a,
E
C_
o
E
i
-J5
U
re
-300
o
E
-250
-200
L
-150
°
C-
-100
.E
-50
z
0
2
6 8
10
12
Time
(weeks)
Fig.
10.
A.
Effect
of
increasing
density
of
Folsomia candida
(collembola) (A
----
)
on
fungal
biomass
(mg
g
litter)
in
microcosms
filled
with
oak
litter.
B.
NH'
-N
leaching
from
oak
litter
(pgg-
litter
wk-l).
O-
=
with
animals,
O-O
=
without
animals.
(After
Anderson
&
Ineson
1984)
decreased
fungal biomass, associated
with
an
increased
ammonium
mobiliza-
tion.
This
association
has also
been
found for
the
interaction
collembola-micro-
organisms
at
constant
grazing
intensities: in
microcosm-studies with
15
Tomo-
cerus
minor,
the
microbial activity
(as
CO
2
-production
and
urease activity)
decreased,
whereas
the
ammonium mobilization
increased
(Verhoef
&
Meintser
1990,
Fig.
11).
In
this
study
animal
addition
negatively
influenced
both respiration
and
urease
activity.
In similar microcosm-studies
addition
of
collembola
or
isopods
showed
positive
effects
on
respiration but
negative
ones
on dehydrogenase
and
cellulase
activity
(Teuben
&
Roelofsma
1990).
Small
differences
in
degradation
stage
of
the
pine
needle
litter substrate
may
be
the reason
for
these
differences
(Teuben
&
Roelofsma
1990).
I I I I
I
, I
-
I
CE

187
-
1L0-
o,
0
6
0
-
-
100
X
60-
.
20
20-
._
c
7VV-
m
E
-
=a
700-
z
I
-
,
500-
'
300-
n
,-
100
-
I
7
6
-
E
0,
10
6-
E
C3
0
2
4
6
8
10
12
Time
(weeks)
Fig.
11.
Effects
of
constant
grazing
intensity
of
Tomocerus
minor
(collembola)
in
microcosms
filled
with coniferous litter.
A:
on
microbial
activity,
measured
as
cumulative
CO
2
production
(pl.
g
d.m.
h-').
B:
on
microbial
activity
measured
as
cumulative
urease
activity,
according
to
Hoffman
and
Teicher
(1961)
(pg
NH
3
-N
g-'
d.m.
3h -').
C:
on
cumulative
NH
-N
leaching
(mol.g
'
d.m.)
o0-
=
without
animals,
e-·
=
with
15
animals,
A-A
=
with
50
animals.
(From
Verhoef
&
Meintser
1990)
n,~~~~~~~~~~~~
Ur/
I
CE
I
on
C(
E
2
1

188
Three-component
interactions
Studies
with
more
than
two
interactive
components
are
more
natural but
also
more
difficult
to
interpret,
whereas
the
effects
of
animal
addition
on
decomposi-
tion
are
often
insignificant
or
inconclusive
(see
e.g.
Bth
et
al.
1981).
In
microcosm-experiments
with
barley
straw
as
substrate
and
with
microflora,
protozoa
and
collembola
(Folsomia
fimetaria
(L.)),
no
significant
effects
were
found
in
respiration,
mass
loss
or
microbial biomass
by
addition
of
collembola
(Andren
&
Schnirer
1985).
In
microcosm-studies
with
both protozoa
and
nematodes
present, metabolic
activity
(as
CO2-production)
was
enhanced
in
comparison
with
systems
with
one
of
the
grazers
only
(Coleman
et
al.
1978;
Elliott
et
al.
1980).
Similar studies
have
been
performed
with
various
combinations
of
bacteria
(B),
protozoa
(P),
bacterivorous
nematodes (N)
and
bacterivorous
mites
(His-
tiostoma litorale,
M)
in
relation
to
nitrogen
mineralization (Brussaard
et
al.
1990).
A
combination
of
protozoa
and nematodes (BPN)
increased
nitrogen
mineralization
as
compared
with
protozoa-only
(BP).
Replacing
nematodes
by
mites
(BPM)
did
not
yield
a significant increase
in
nitrogen
mineralization
as
compared
with
the
protozoa-only treatment
(BP).
In
comparison
with
the
protozoa-only treatment
(BP)
the
nitrogen
mineralization
was
significantly
enhanced
with
both
nematodes
and
mites
present (BPNM,
P
<
0.05),
but
not
to
the
same
extent
as
in
the
treatment
with
nematodes
as
the only grazers
besides
protozoa
(BPN,
P
<
0.001).
So
the
mites
counteracted
to
some
extent
the
effect
of
nematodes.
In
agreement
with
this
result,
numbers
of
nematodes
were
signifi-
cantly
lower
in
the
presence
of
the
mites
(BPNM;
P
<
0.01),
whereas
those of
amoebae
were
significantly
higher
(BPM
and
BPNM)
than
in
the
absence
of
the
mites
(BP
and
BPN;
P
<
0.001).
It
was
calculated
that
1
g
of
mite
C.g
-'
soil
caused
a
25
g
increase
in
amoebal
C.g-
soil.
Perhaps the
filter feeding
activity
of
the
mites increases
the
encounter
rate
between
amoebae
and
bacteria,
leading
to
an
increased
amoebal growth
rate.
In
general, the
results
of
microcosm-studies carried
out
under
conditions
of
nitrogen
limitation
and
in
the absence
of
overgrazing
agree
with
the
conceptual
model
given
in
Fig.
12
(Anderson
et
al.
1981).
Multi-component
interactions
An
important
question
is
whether
the observed
effects
of
faunal
activity
in
microcosm
and
pot
experiments
also
occur
under multi-component
field
con-
ditions.
Field
research
during
the
fallow
part
of
a
wheat-fallow
cropping
system
allowed
the
study
of
mineralization
by
the
fauna
because
of
the
absence
of
plants
taking
up
the
nutrients. Temporal
displacement
of
peak
biomass
of
primary
decomposers,
their
grazers
and
the
latter's
predators
was
reported
following
an
imposed
pulse
of
rainfall in
a
near-natural
greenhouse
experiment
with
large
cylinders
of
undisturbed
soil
from
the
fallow
part
of
the
rotation
(Elliott
et
al.
1986).
These
results confirmed
those
obtained
under
real
field

189
1
2
4
N
I.-
co
4
U
0
Time
(days)-----*
Fig.
12.
Conceptual
model
of
substrate
utilization
and
nutrient
mineralization
with
and without
grazers.
(From
Anderson
et
al.
1981).
conditions
where
mineralization
rates and nitrogen
concentrations
in
the
soil
coincided with
a
rapid
increase
in
protozoan
biomass,
while
a
clear
temporal
displacement
of
faunal
groups
was
apparent
even
at
sampling intervals
of
3
to
4
weeks.
This
suggested
decomposition
of
lower
trophic
levels'
biomass,
result-
ing
in
net
mineralization (Elliott
et
al.
1984).
Clear
temporal
displacements
of
primary
decomposers, their consumers
and
the
latter's
predators
have
also
been
assessed
following
rainfall
events
in
semi-deserts,
especially
for
the
bacteria-
nematodes-mites food
chain
which
led
to
enhanced
decomposition
and
miner-
alization
as
compared to conditions
without
predators
(Santos
&
Whitford
1981;
Santos
et
al.
1981;
Elkins
&
Whitford
1982;
Whitford
et
al.
1982).
Similar results
were
found
in
natural
(blue
grama)
grasslands:
in
spring,
protozoa
and nematodes
increased
concomitantly
with
bacteria
and
fungi;
the
fauna
subsequently reduced their food
sources
which
coincided with
an
increase
of
soil
inorganic nitrogen
(Ingham
et
al.
1986a).
This
was
not
observed
follow-
ing
an
increase
of
bacteria
during
autumn,
suggesting
that
during
that
period of
the
year
the
nitrogen
was
immobilized
in
the microflora
and/or
the
plants took
benefit
from
the
mineralized
nitrogen.
There
is
evidence
that
plants
indeed
benefit
from
the increased
nitrogen
mineralization
by
the
fauna.
Higher
shoot
biomass
and
N
contents
of
shoots
of
plants
growing
in
the
presence
of protozoa
and
nematodes
as
compared
with
plants
growing
without
fauna
were
often
found (Woods
et
al.
1982;
Clarholm
1985;
Ingham
et
al.
1985;
Kuikman
&
van
Veen
1989).
Both rhizosphere
and
non-rhizosphere nematodes
may
contribute
to
the observed
effect
when
plants
are
grown
in
soil.
However,
pot
experiments
with
nitrogen
limited
spring
wheat
grown
in
perlite
showed
that
between
4
and
8
weeks
after
the
start
of
the
experiment
nematode
numbers
averaged
about
260g
'
fresh
roots and
only
4.7
g ' perlite.
The
shoots
of
the
wheat
plants contained
slightly
but
significantly
(P
<0.05)
more
nitrogen
in
the
pots
with
nematodes
as
compared
to those
without
(Bouwman
et
al.
pers. comm.
1989).

190
Fig.
13.
Set-up
of
an
enclosure experiment
in
the
field.
L,
litter;
PT, plastic
tubes;
S,
strip
with
glue;
SE,
stainless
steel
enclosures.
A
gauze
net
was
spread
over the plastic tube-frame
(:
not
on
drawing).
Further
evidence
for
animal mediated
nitrogen
availability
for plants
comes
from
field
studies
with
lysimeters
with
and
without
plants
in
the
absence
or
presence
of
soil
animals (Anderson
et
al.
1985;
Verhoef
et
al.
in
prep.). They
show
that
the
surplus inorganic nitrogen
mobilized
in
the
presence
of
soil
animals
without
plants
disappears
in
lysimeters
with
plants.
In
field
studies
in
a
Pinus
nigra
forest,
the
density
of
the
dominant
collem-
bolan
Tomocerus
minor
was
manipulated
in
enclosure
experiments
(Fig.
13).
It
was
shown
that
at
high
densities
(approximately
4,000
individuals
m- 2 ) the
nitrogen
concentration
of
the
F
layer
became
2.3
times
as
high as
that
of
the
same
layer
in
defaunated plots
(Verhoef
&
de
Goede
1985).
Similar
findings
of
microbial
nitrogen
immobilization
in
the
presence
of
high
numbers
of
micro-
bivorous animals
have
been
shown
in
microcosms
containing
Scots
pine
seed-
lings
(Baath
et
al.
1978).
According
to
these
authors
this
is
due
to the
high
effectiveness
of
the
internal circulation
of
nitrogen
between
the
soil
organisms,
being
superior
to
root
uptake.
These
studies
indicate
that
the
contribution
of
functional
groups
of
soil
animals
to
decomposition and mineralization
depends
on
their
population
density,
which
can
fluctuate
considerably
even
over
short
time
periods.
Paradoxically,
the
decomposition rate
of
organic
matter
can
often
be
des-
cribed
by
simple
first-order
kinetics
(Janssen
1984;
Andren
et
al.
1988)
without
considering
organism
dynamics. In fact,
total
organism
biomass,
including
bacterial
and
fungal
biomass, may
be
a
poor
indicator
of
biological
activity.
Rather than
pointing
to
the
low
importance
of
the
fauna
at
the
observed
level
of
microbial biomass,
this
may instead indicate
that
the
microbial biomass
is
kept
at
a
low
level
by
microbial
grazers
(Andren
et
al.
1988).
In
their
turn,
the
grazers
may
not
build up
a
large
biomass,
but
instead
be
consumed
by
predators
(Elliott
et
al.
1988).
Hence,
it
appears
that
in
a
variety
of
ecosystems,
microbial
grazers
and
their
predators
significantly
contribute
to
the
mineralization
of
nitrogen,
despite
their
often
low
biomass.
This
may
well
be
due
to
the
rapid
replacement
among
the
various functional
groups
of
decomposers,
their
grazers
and
the
latter's
predators,
whereby
patterns
in
nitrogen
dynamics remain
the
same
(Ingham
et
al.
1986b).
A
common
feature
of
these
studies
is
that
most
of
the
effects
of
biological
interactions
on
decomposition
and
mineralization
becomes
apparent
after
im-
posed changes
of
the
densities
of
functional
groups,
e.g.
by
drying-rewetting
or
eliminating/adding
animals.

191
Nitrate
leaching
(umol
g'dm)
Time
(months)
Fig.
14.
Nitrate
leaching
from
lysimeters
in
a
Pinus
nigra
stand
with
(0-)
and
without
(-O)
meso-
and
macrofauna.
In
field
studies
under
natural
conditions
in
coniferous forest
soils
meso-
and
macrofauna
significantly
increased
nitrate
mobilization
in
autumn
(F1
.
48
=
6.02;
P
<
0.05).
In
summer
there
was
no
significant
effect
(Verhoef
et
al.
in
prep.;
Fig.
14).
In
the
same
habitat,
collembola
have
an
immobilizing
effect
on
nitrogen mobilization
in
winter (Verhoef
&
de
Goede
1985).
Hence, it
would
appear
that
under
natural
conditions
in
a pine
forest
the
nitrogen mobilization
by
the
fauna
to
some
extent
was
synchronized
with
plant
demand,
whereas
during
winter
soil
animals
such as
collembola,
reduce
nitrogen
losses
from
the
system.
In microcosm
studies
with
litter
similar buffering
effects
by
collembola
and
isopods
have been
found
concerning
the
concentrations
of
exchangeable
nutrients
such as
calcium,
magnesium
and
nitrate
(Teuben
&
Roelofsma
1990).
If
additional
studies confirm
the
generality
of
these
observations,
a
thorough
understanding
of
biological
functions, interactions
and
processes
within the
soil
community
is
required
for
predicting
the
impact
of
perturbations
of
natural
ecosystems.
Soil
ecological
knowledge
would
also
be
necessary
for
improving
the
organic
matter
status
and
nutrient
economy
of
perturbed
systems
such
as
those
in
forestry
and
agriculture. Therefore
we
will
henceforth
discuss
the
impact
of
some
abiotic
soil
factors
(temperature,
moisture),
and
management
(fertilization, harvesting,
litter/crop
residue
addition
and
placement) on
sea-
sonal
patterns
of
soil
animal
activity
and
the associated
dynamics
of
organic
matter
and
nitrogen.
5.
Effects
of
abiotic conditions
on
animal-mediated
decomposition
and
mineralization
processes
Soil
temperature
and moisture
and
to
a
lesser
extent resource
quality
have
been
found
to
influence
the seasonal
nitrogen mineralization
in
forest
soils
(Vitousek

192
6
5
4
E
-a3
' 2
E
1
ZL
5
E4
c
3
E
E
2
1
0
2
4
6
8
10
12
Time
(weeks)
Fig.
15.
Ammonium
leaching
from
microcosms
filled
with
F
layer
material
from
Pinus
nigra,
calculated
per
unit
mass
of
substrate,
per
two
weeks.
0-0
=
with
Tomocerus
minor,
-o
=
mi-
croorganisms
only.
(A)
at constant
19
0
C
(B)
at
dielly
fluctuating
10/19°C.
&
Matson
1985).
During
periods
with
increasing
temperatures
and
relatively
high
moisture, mineralization
increases,
whereas
in
spite
of
high
temperatures
mineralization
decreases when
the
soil
is
dry.
Optimal temperatures
for
nitrogen mineralization
have been assessed
in field
and
laboratory
studies
with
organic
soil
layers
(Anderson
et
al.
1983;
Verhoef
&
de
Goede
1985),
the
optima
being
different
for the
different
soil
horizons.
At
dielly
fluctuating
temperatures
(10-19°C)
the
ammonium
mobilization
from
pine
litter
showed
a
constant pattern
over
a
period
of
several weeks,
whereas
at
a
constantly
high
temperature
(19
°
C)
mineralization
was
rapid
but short
(Ver-
hoef
&
Meintser
1990;
Fig.
15).
Relatively
high
decomposition rates
of
organic
material during
colder
seasons
(late
autumn
to
early
spring)
(cf.
Bleak
1970;
Hagvar
&
Kj6ndal
1981;
Vogt
et
al.
1983;
Verhoef
&
de
Goede
1985)
could
be
attributed
to temperatures
fluc-
tuating
around
0°
C.
The
repeated
freezing
and
thawing
of
leaves
could
cause
fragmentation,
increased
leaching
and/or
enhanced
accessibility
to
microbial
attack
(McBrayer
&
Cromack
1980;
Berg
et
al.
1982;
Staaf
&
Berg
1982).
However, recent studies
on
the
effects
of
repeated
freezing
and
thawing
on
rates
of
decomposition
in
aspen
and
pine
litter
have shown
that
simple freezing
and
- I

193
-o
O
E
Time
(days)
Fig.
16.
Effect
of
soil
moisture
(%
w/w)
on the
population
growth
of
the
flagellate
protozoan
Cercomonas
sp.
growing on
Pseudomonasfluorescens
at
200
C
in
a
microcosm experiment
with
silt
loam
soil.
(From
Zwart
et al.
in
prep.)
decomposer
activities
beneath
the
snow are
more
important
factors
in
hibernal
litter
decomposition
than
freeze-thaw
cycles
(Taylor
&
Parkinson
1988).
While
the
pattern
of
change
in
soil
temperature
in
the
course
of
the
day or
the
season
is
rather
predictable,
this
is
far
less so
with
changes
in
soil
moisture.
Various
studies
have
been
aimed
at
quantifying
the
effects
of
soil
moisture
on
the
activity
of
soil
animals
and
nutrient
dynamics.
It
is
obvious
that
animals
living
in
water-filled
pores
and
water
films
around
soil
particles
(such
as
pro-
tozoa and
nematodes)
are
sensitive
to
desiccation.
Studies
on
the
growth
of
flagellates
in
microcosms with
silt
loam
soil
showed
a
sharp
boundary
between
the
soil
moisture
contents
where
the
protozoa
hardly
showed any
growth
(11.4%
w/w)
and
most
rapid growth
(18.6%
w/w)
(Zwart
et
al.
in
prep.;
Fig.
16).
In
another
microcosm-experiment
a
silt
loam
was
incubated
under moisture
conditions
ranging
from
14.4
to
19.5%
(w/w)
after
amendment
with
lucerne
meal
and numbers
of
nematodes
belonging to
various
functional groups
were
counted after
six
months
(Bouwman
in
prep.; Table
3).
Here
again,
clear
boundaries
of
activity
were
assessed
for
some
quantitatively
important
bacter-
ivores
(Rhabditidae) and
fungivores
(Aphelenchida),
but
others
(bacterivorous
Cephalobidae) appeared
unaffected.
Although
increases
in
numbers
of
protozoa
and bacterivorous
nematodes
have been
observed
in
the
field
or
in
field
experi-
ments
following
rewetting
of
dried
soil
(Elliott
&
Coleman
1977;
Clarholm
1985;
Schntirer
et
al.
1986)
these
results
are
difficult
to
interpret
quantitatively
in
terms
of
decomposition
and
mineralization
without
estimates
of
physiological
activity
and
population
turnover.
In various
studies, however,
soil
faunal
activity
under
moisture
stress
has
been
reported
as
important
for
continued
decomposition
and
mineralization.
In
a
soil
microcosm-experiment
with
plants
the
interaction
between
S'N-labelled
bacteria
--
A
A

194
Table
3.
Effect
of
soil
moisture
(%
w/w)
on
numbers.
100
g-'
soil
of
various
groups
of
nematodes,
after
six
months
of
incubation
at
150
C
in
soil
microcosms
with
silt
loam
soil
amended
with lucerne
meal.
Moisture
Bacterivores
Fungivores Omnivores
(%
w/w)
Rhabditis
Cephalobidae
Aphelenchida
Tylenchus
Dorylaimida
14.4-15.6
175
a
932
a
311
a
99
a
317a
15.6-16.7
255a
b
907
a
150
a b
70
a1 68 '
b
16.7-17.6
6 72
b
1008
a42b '
61
a128
b
17.6-19.5
1236'
954
a80¢
24
a
222
b
Figures
followed
by
different
symbols are
significantly
different (P
<
0.05).
Statistical
analysis
carried
out
on
log-transformed
data.
(From
Bouwman
in
prep.)
and
protozoa
was
studied,
as
affected
by
moistening
the
soil
every
first, second
or third
day.
In
soils
with
bacteria
only
significantly
less
(P
<
0.05)
nitrogen
was
taken
up
by
the
plants
if
the
soil
was
moistened
every
second
or
third
day
as
compared
with
daily
water additions.
In
the
presence
of
protozoa
nitrogen
uptake
in-
creased
(P
<
0.01)
by
5,
10
and
18%
at
moistening
the
soil
every
day,
every
second
and
every
third
day,
respectively.
This
was
accounted
for
by
increased
uptake
of
bacterial
'
5
N,
apparently
made
available
by
protozoan
grazing
(Kuik-
man
et
al.
1989;
Fig.
17).
Microarthropods
also,
have been
reported
to
release
the
decomposition
of
organic
matter
from
environmental
stress
under
certain
field
conditions.
After
exclusion
of
mites,
seven
abiotic
factors explained
80-90%
of
the
variation
in
organic
matter
decomposition,
whereas
only
50% was
explained
by
these
fac-
tors
in
the
presence
of
mites,
particularly
nematode-feeding Tydeidae
(Santos
&
N.
z
a
M
.0
0
II
0J
0
W
Cr
di
36
days
2 1 2
3
Time
days)
between
water
supply
Fig.
17.
Recovery
of
bacterial
'
5
N-nitrogen
in
plant
nitrogen
as
a
percentage
of
the
inoculated
amount
at
three
soil
moisture
regimes
and
two
sampling
dates
in
a
microcosm
(day:
14
h
light,
200
C;
night:
160
C)
experiment.
bacteria: i,
bacteria
and protozoa:
a
(From Kuikman
et
al.
1989).

195
Whitford
1981;
Santos
et
al.
1981).
Similar
results
were
reported
for
mesostig-
matid
mites
(Elkins &
Whitford
1982).
These
studies
were
carried
out
in
semi-
deserts
where
soil
moisture
is
the
most
important
limiting
factor
for
decom-
posers
as
long
as
sufficient
organic
matter
is
available.
No
such
effects
were
reported
in
these
studies
for
fungivorous nematodes
or
mites
during
later
stages
of
decomposition,
possibly due
to
the
low
productivity
of
the
system as
com-
pared
to
the early
bacterial-dominated
stage
of
decomposition.
In
another
study
by
Persson
(1989),
organic
matter
decomposition,
measured
as
CO2-evolution
and
net
nitrogen mineralization
were
measured
in
F/H
layer
materials from
a
Swedish
spruce
stand under
various
combinations
of
temperature
(5
and
15
°
C)
and moisture
(15,
30
and
60%
WHC).
Addition
of
a mixed,
mainly
micro-
arthropod,
soil
fauna
did
not
change
the
CO2-evolution
as
compared
to
a
defaunated
variant
(cf.
Andr6n
& Schniirer
1985).
However,
it significantly
increased
net
nitrogen mineralization for
each
of
the
combinations
of
tem-
perature
and moisture conditions.
The
increase was
dependent
on
soil
tem-
perature,
but not
on
soil
moisture.
Because
the net
nitrogen
mineralization
in
the
absence
of
the
arthropods
was
dependent
on
both
temperature and
mois-
ture,
it
was
concluded
that
the
arthropods
were
important
for
switching
from
immobilization to mobilization
of
nitrogen
in
maintaining
net
nitrogen
miner-
alization
under
dry
conditions.
Hence,
it
would
appear
that
while
under
the
development
of
moisture
stress
bacterial
and
subsequently
fungal
decomposition
and
nitrogen mineralization
are
slowed
down
and
finally
inhibited,
these processes are
to
some
extent
continued
under
moisture
stress
in
the
presence
of
the
soil
micro-and
meso-
fauna.
6.
Effects
of
management
on
animal-mediated
decomposition and
mineralization
processes
Fertilization
In textbooks
it
is
generally
stated
that
input
of
nutrients
into
a
nutrient
deficient
system leads
to
increasing
decomposition
rates. The
addition
of
nitrogen,
e.g.,
to
a
shortgrass
prairie,
a
mountain
meadow
and
a
lodgepole
pine
forest
in-
creased
decomposition rates
with
5,
21
and
13%,
respectively,
relative
to
the
controls
(Hunt
et
al.
1988;
Table
4).
Primary
production
showed
a greater
response to
nitrogen
fertilization
than
did decomposition,
suggesting
that
pri-
mary
production
is
the
more
nitrogen
limited
process.
However,
many
examples exist
in
which
addition
of
nitrogen
to nitrogen
deficient
systems (with
high
C/N
ratio)
slows
down
decomposition,
especially
if
it
concerns
recalcitrant
organic
material
(Fog
1988).
For
pine
needle
litter,
e.g.,
decomposition
rate
is
mainly
governed
by
the
rate
of
lignin
decomposition
(Berg
1986)
and
this
rate
is
decreased
by
nitrogen addition.
The
ligninolysis, a
process
in
which
various
basidiomycetes are involved,
appears
to
be
inhibited
by
the
addition
of
nitrogen
(e.g.
Arnolds
1988).

196
Table
4.
Effects
of
addition
of
nitrogen
to
three
ecosystems.
Ecosystem
Variable
Prairie
Meadow
Forest
Percent
increase
over
control
Plant production*
81
102
52
Plant
N content**
56
39
24
Decomposition
rate***
5
21
13
Litter
N
content***
20
11
29
*Aboveground standing
crop after
the
growing
season
in
grasslands
and
radial
increment
in
forest.
**Live
shoots
in
grasslands
and
live
needles
in
forest.
***Of
litter
placed
in
its
system
of
origin.
(From
Hunt
et
al.
1988)
Similar
effects
were
found
in
microcosm-studies
with
Pinus
nigra
litter,
to
which
nitrogen
was
added
as
NH
3
(Verhoef
&
Meintser
1990).
The
organic
material
was
from the
F
layer
with a
low
C/N
ratio. Continuous
supply
of
nitrogen
decreased
decomposition
rate
and
the
stimulatory
effect
of
the
collem-
bolan
Tomocerus
minor
on
nitrogen mobilization
(Table
5).
It
is
noteworthy
that
in
microcosms,
filled
with
F
layer
material
from areas
with
a high
nitrogen
input
from atmospheric deposition
(up
to
50
kg
ha-
yr
')
after
two
months
at
19°C
without
further
nitrogen
input,
the
excess
nitrogen
has
been
mobilized
and
leached
out,
whereas the
decomposition
rate
had
increased
to
control
values
(Verhoef
&
Dorel
1988;
Verhoef
&
Meintser
1990).
Thus
it
can
be
concluded
that
addition
of
nutrients
to
nutrient
deficient
systems
can
have negative
effects
on
certain microorganisms
causing
shifts
in
microbial
composition,
which negatively
affects
soil
fauna
(Fog
1988).
As
a
result
decomposition
and
mineralization
rate
may
decrease.
In
agriculture,
with the
current
emphasis
on
reduced
input
farming,
fertiliza-
tion
is
reduced
or
left
behind
as
an
experimental
treatment
in
research projects.
In
Swedish
arable land
no
significant
differences
were
assessed
for
biomass
of
protozoa
and
numbers
and
biomass
of
nematodes,
mites,
collembola,
enchy-
traeids
(with
the
exception
of
two
years)
and
earthworms
between
unfertilized
spring barley
and
barley
receiving
120
kg
N
ha-',
but
significant
differences
were
found
at
lower
taxonomic
levels
of
these
groups
and
on
specific
sampling
occasions (Andr6n
et
al.
1988;
Hansson
et
al.
1990).
Table
5.
Effects
of
addition
of
nitrogen
to
pine
needle
litter
Variable
Control
+
NH
3
(150
ppb)
Decomposition
rate*
12.0%
8.3%
Animal-stimulated
N
mobilization**
54.0% 32.0%
*Dry
mass
loss
over
12
weeks
at 10/19°C
**Percent
increase
in presence
of
15
Tomocerus
minor
over
total
inorganic
N
mobilization
with
microorganisms
only.
(From
Verhoef
&
Meintser
1990)

197
Effects
of
the
kind
of
nutrients
added
on
soil
fauna
can
be
derived
from
a
study
on
arable
land
in
a
Dutch
polder
soil.
In
one
of
two
arable farming
systems
average
amounts
of
5650kg organic
matter
ha-'
1
yr
- '
were
added
as
farmyard manure, crop
residues
and
green
manure
during
thirty
years.
In
the
other
system
on
average
3200
kg
ha-
'
yr
'
was
added
as
crop
residues only
and
extra
nutrients
given
with
the
organic
matter
in
the
first
system,
were
compen-
sated
for
by
artificial fertilizer
additions
in
the second
system
(for details
see
Kooistra
et
al.
1989).
After the
treatment
period
of
30
years
soil
animals
were
sampled
during
the
growing
season
when
amounts
of
mineral
nitrogen
available
to
the
winter wheat
crop
were
similar.
Here
again,
no
differences
in
protozoa,
nematodes,
mites,
collembola
and
enchytraeid
biomass
were
assessed
between
the
treatments
(Fig.
9).
Differences
for earthworms
were
mainly
due
to
the
unique
colonization
history
of
the
site
for
this
group.
There
were,
however,
important
differences
at
lower
taxonomic
levels
of
microarthropods
between
the
two
systems
(Brussaard
et
al.
1988;
Table
6).
It
seems
to
be
still
open
for
research
whether
the
clear
differences in
species
diversity
and
abundance
within
the
various
taxonomic
families
and
orders
of
soil
animals
which have come
about
under
the
influence
of
fertilization
and manuring
affect
decomposition
and
nutrient
mineralization
to
a
measurable
extent.
Harvesting
and
addition
of
harvest
residues
Many
studies
of
the
direct
effects
of
forest
cutting
have
shown
changes
in
chemical
and
physical
factors,
nutrient
supply,
root
dynamics,
decomposition
rate
and
soil
biota
(BAAth
1980;
Vitousek
&
Matson
1985;
Huhta
1971;
Seastedt
& Crossley
1981).
The
impact
of
these
changes
strongly
depends
on the
utiliza-
tion
intensity. In
conventional
stem
harvesting
only
large
logs
are
utilized,
leaving
much or
even
most
of
the forest
biomass on
the
site.
This results
in
only
small
withdrawals
of
nutrients and
relatively
small
changes
in
chemical
and
physical
factors,
decomposition rate
and
soil
biota.
However,
"complete-tree
harvesting",
in
which
tree
stumps,
root
systems
and
foliage
are
harvested has
great
effects
(Young
1968;
Kimmins
1987)
and
a
shift
from conventional
to
complete-tree
harvesting
shows
strong
increases
in
removal
of
plant nutrients
(Kimmins
1987).
Harvesting
of
stumps
and
root
systems
greatly changes the
whole
soil
system,
causing
a
thorough
mix
of
the
soil
and
a
disappearance
of
the
structure
of
the
organic
soil
layer.
Apart
from
that,
stumps
are
considered
refugia
for
all
types
of
soil
animals
directly
after
tree
harvesting, from
which
the
soil
layers
can
be
recolonized
(Ehnstr6m
1984).
The
input
of
harvest
residues
may
be
beneficial in
terms
of
nutrient
supply,
but
this
depends strongly
on
the
chemical
composition
of
the
material.
Green
foliage
and
fine
twigs
contain
readily
decomposable
tissues,
relatively
rich
in
nutrients.
If
they
remain on the
forest
floor
as
harvest
residues,
together
with
the
soil
organic
layer, the
fungi
present
in
these layers
may
temporarily
immobilize
nutrients,
preventing
premature
nutrient
flush.
These
immobilizing
effects
can
be
augmented
by
fungivorous
soil
animals
(cf.
Verhoef
&
de
Goede
1985).

198
Table
6.
The
12
most
abundant
taxa
of
mites
and
collembola
from
the
layers
0-5,
7.5-10,
15-17.5
and
22.5-25
cm
below
the
surface
of
two
fields
differing
in
organic
matter
content
of
the
topsoil
(A:
2.8%;
B:
2.2%)
as
a
consequence
of
32
years
of
differential
manuring.
Sums
of
six
soil
cores
(diameter
6cm)
per
date
per
field.
Taxon
18
Apr.
19
Jun.
30
Jul.
19
Aug.
18
Nov.
Total
for
1986
Associated
with
a
relatively
high
organic
matter
content (A:
2.8%)
Friesea mirabilis
Tullbergia
quadrispina
Tullbergia
krausbaueri
Onychiurus
armatus
A
9
4 55
8
35
111
B
0 0
0
0
0
0
A
24
2
16
19
45
106
B
1 0
0
0
0
1
A
16
15
115
99
151
396
B 3
16 16
46
8 89
A
34
47
170
31
56
338
B 6
21 61
4 0 92
Associated
with
a
relatively
low
organic
matter
content
(B:
2.2%)
Eupodidae
Pyemotidae
Alliphis
halleri
Tarsonemidae
Folsomia
candida
Histiostoma
litorale
Arctoseius
cetratus
Hypogastrura
denticulata
A
5
11
52
13
21
102
B
1
100
55
27
3
186
A
7
20
88
34
89
238
B
10
144
80
196 23
453
A
40
13
20
5
10
88
B
8
150
34
39
2
233
A
2 1
10
4
11
28
B
4
8
23
60
17
112
A
18
9
16
4
18
65
B
2
237
68
38
6
351
A
24
11
23
11
21
90
B
4
501
59
9
0
573
A
0 3 1
0
1
5
B
0
71
63
20
0
154
A
0 6 2 1
0
9
B 0
25
137
251
21
434
*crop:
winter
wheat
soil:
sandy
loam,
pH-KCI
7.5
(After
Brussaard et
al.
1988)
Few studies
have
analyzed
soil
surface
organic
matter
dynamics on
a
single
site
after harvesting, combined
with
changes
in
decomposition rate, nitrogen
dynamics
and
soil
fauna.
In
a
recent
study
in a
native
hardwood
forest
of
Quercus,
Carya
and
Acer
spp.
(Blair
& Crossley
1988)
data
on
decomposition
rates,
nitrogen
dynamics
and
microarthropod
densities
in
a
watershed
up
to
its
eighth
year
of
regrowth
following
clearcutting
were
compared
with
data
from
an
adjacent
uncut
refer-
ence
watershed.
In
the
first
year
following
clearcutting the
mean
annual
density
of
total
litter
microarthropods
was
reduced
with
over
50%,
relative
to
the
uncut
reference

199
Table
7.
Seasonal
means
of
maximum
and
minimum
soil
temperatures
(C)
in
an unthinned
reference site
and
a
thinned
site.
Unthinned
site
Thinned
site
Spring Summer
Autumn
Winter*
Spring Summer
Autumn
Winter*
max.
10.5
15.1
14.3
10.3
12.3
17.4 15.2
10.2
Temperature
min.
4.6
10.9
9.3
4.7
4.3
11.5
10.7
6.3
Means
are
based
on
10
recording intervals
per
season,
recorded
in
the
litter
layer.
*Winter
data
are based
on
recordings
in
December
only.
(From
Verhoef
et
al
in
prep.)
site.
The
pattern
of
seasonal
abundance
was
also
changed
from
a
unimodal
curve
(with
maximal summer
densities) in the
uncut
reference site
to a
bimodal
curve
(with a
spring-
and
an
autumn
peak)
in
the
cut
site.
This
was
presumably
caused
by
high
summer
temperatures
and
reduced
litter moisture. Eight
years
after cutting
mean
annual
densities
were
still
lower
than
those
of
the
reference
site.
The
bimodal
curve,
however,
had
been
changed
into
a
unimodal
one.
These
effects
were
probably
strongly
linked
with
the changed microclimatological
conditions
after cutting. Decomposition
rates
were
slowed
down
in
the cut
site,
whereas
slower increases
in
nitrogen
concentration
and
lower
levels
of
immobil-
ization
were
observed
in
the cut
site,
relative
to
the
uncut
site.
This may indicate
that
the
reduced
microarthropod
densities
were
related
to
changes
in
decom-
position
and
nutrient
dynamics
following
clearcutting.
The
data
on
decreasing
decomposition
and
nutrient concentration
are
in
contrast
with results showing increasing
decomposition
at
increased tem-
peratures
and
AET
following
clearcutting
(Meentemeyer
1978;
Meentemeyer &
Berg
1986).
This
contradiction
can
be
explained
by
the
conditions
prior
to
felling in
the
forest.
In
forests with
relatively
low
decomposition
rates,
low
densities
of
soil
biota
and
a
cold climate
(as
in
large
parts
of
Swedish
boreal
forests)
canopy
removal
increases
insolation,
leading
to
improved
conditions
for
both
soil
biota
and
decomposition.
In the
above-mentioned
hardwood
forest,
conditions
under
a
closed
canopy
apparently
were
favourable for
primary
(bacteria and
fungi)
and
secondary decomposers
(microarthropods,
nematodes,
etc.)
and decomposition.
Canopy
removal
created
sub-optimal
conditions
by
increasing
temperature
extremes
and
moisture
stress.
Similar results
were
found
in a
study
on
the
effects
of
thinning
in
a
temperate
Pinus nigra
forest. One
site
was
thinned
20%
in
a
regular
way,
and an
adjacent
unthinned
site
was
used as
a
reference.
During
a
ten
months'
period,
four
years
after
thinning,
temperature
extremes,
water
economy,
faunal
densities
and
diversities
were
established. In
lysimeters
decomposition rates
of
the
organic
layer
and
nitrogen mobilization
were
established (Verhoef
et
al.
in
prep.).
Thinning
caused
an
increase
in
temperature
extremes
(Table
7).
In
general,
evaporation
from the
soil was
higher
in
the
thinned
site,
whereas
evaporation
from the
canopy
was
higher
in
the
unthinned
site.
The
density
of
the
total
soil
fauna
was
higher (up
to
53%)
in
the
reference
site
compared
with
the
thinned

200
site.
The
difference
was
caused
by
reproduction
peaks
of
collembola
and
mites
in
the
reference
site.
The
diversity
indices
were
similar
for
both
sites.
Decom-
position
of
the
litter
layer
in
the
thinned
site
was
17%
lower
compared
to
the
reference
site.
Total
mineral
nitrogen
in
the
thinned
site
was
39%
lower
com-
pared to
the
reference
site,
whereas
total
nitrogen mobilization
was
30%
lower
(Verhoef
et
al.
in
prep.).
This
study,
too,
showed
that
harvesting
can create
sub-optimal
conditions.
However,
the
effects
of
this
form
of
perturbation
depend
not
only
on
the
perturbation
itself,
but
also
on
the
conditions
prior
to
the
perturbation.
Agricultural
systems
are
perturbed
systems
by
their
very
nature,
but
harvest-
ing,
especially
of
annual
crops,
has
a
relatively
strong impact
on decomposition
and
mineralization
because
of
the
rapid
dying-off
of roots
and
because it
is
usually
associated with
the
addition
of
crop
residues
to
the
soil.
The
pattern
of
decomposition
and
the
speed
at
which
it
proceeds
have been
reported to
relate
to the
placement
of
the
litter.
Various
studies
have
shown
that
organic
carbon
and
nitrogen accumulate
in the
top
10cm
under
no-till
or
minimum
tillage as
compared
with
conventional
tillage
(Westmaas
Research
Group
on
New Tillage
Systems
1984;
House
et
al.
1984;
Juma
&
McGill
1986).
Few
studies,
however, have
analyzed
these
effects in
terms
of
the
associated
changes
in
the
microbial
and
faunal
community,
and
the
dynamics
of
organic
matter
and
nitrogen.
The
depth
distribution
of
fungal
biomass on
winter
wheat
straw
residues placed
on
or
incorporated
in
a
clay
loam
soil
indicated
that
fungi
may
be
important
decomposers
of
surface
straw
and
less
so
of
incorporated
straw.
Fungal
biomass
increased
with
increasing
nitrogen
fertilization
at
the
time
of
residue
placement. The
fungi
may
have
been
able
to
use
the
surface
straw
carbon and
translocate
the
soil
nitrogen
with
their
extensive
hyphal
network
(Holland
&
Coleman
1987).
Moreover,
microbial biomass
carbon
and
nitrogen
and
microbial
activity,
measured
as
1
4
C
taken up
from
labelled
straw
and
as
cumulative
CO
2
respired,
were
higher
in
the
incorporated-straw treatment than
in
the
surface-straw
treatment,
which
indicates
a
more rapid
decomposition
of
organic
carbon.
Although
soil
nitrogen
availability
had
no
significant
effect
on
the
decomposition
rate
of
either
the
surface
litter
or incorporated
litter,
micro-
bial
biomass
carbon
of
incorporated
straw and cumulative
CO
2respired
were
lowest
in
the
low-nitrogen
treatment.
In
the
surface
straw microbial biomass
carbon
increased
as
nitrogen
availability
increased,
but
cumulative
CO
2respired
decreased.
This
suggests
that
the
total
microbial
community
of
surface
straw
became increasingly
efficient
at
carbon
utilisation
as
nitrogen
availability
and
the
proportion of
fungal
biomass
increased.
This
agrees
with
the
known
high
assimilation
efficiency
of
fungi
for
carbon
as
compared
to
bacteria and
was
confirmed
by
the higher percentage
of
14
C
from
labelled
residue
retained
in
the
microbial biomass
in
the
surface-straw
treatment
than
that
in
the
incorporated-straw
treatment.
Also
the microbial
biomass
will
have
turned
over
more
slowly
with the increasing
importance
of
fungi
as
a
component
of
the
microflora.
At
the
same
time
maximum
net
nitrogen
im-
mobilization
was
higher
in
the
surface
straw
than
in
the
incorporated
straw.
It

201
was
concluded
that
the microbial
community structure
can
control carbon
retention
in
ecosystems
and
that
no-till
systems
may
conserve
organic
matter
because
of
a
higher
proportion
of
fungi
and
hence
a
higher
substrate
use
efficiency
(Holland
&
Coleman
1987).
An
alternative,
perhaps
more
realistic
interpretation,
is
that
differences
in
substrate
quality
were
brought
about
by
adding
weed
residues with different
C/N
ratios
to
the
surface
rather
than
adding
artificial
fertilizers
as
in
the
above-mentioned
study.
The
weeds
with
the
lower
C/N
ratios
(16
or
17)
decomposed
more rapidly
and
supported
greater
popula-
tions
of
bacteria,
fungi
and
nematodes,
than
the
weed
with
the
higher
C/N
ratio
(29).
One
might
expect
that
in
no-till
agriculture
the
fungivorous
fauna
is
more
numerous
and
more
important
for
mass
and
nutrient
transfer
than
in
the
conventional
tillage systems.
In
spite
of
its
importance
for
the
dynamics
of
organic
matter
the fungal
biomass
in
no-till,
however,
was
not
more
than
twice
as high
(up to
1.8
pg/g
soil) in
surface
straw
as
in
incorporated
straw
in
a
laboratory
experiment
and
its
biomass
was
less
than
1 %
of
that
of
bacteria
in
all
cases
(Holland
&
Coleman
1987).
As
mentioned
earlier
in
the
text,
this
may
either
mean
that
fungivores
are
not
important
or,
in
contrast,
that
they
exert a
heavy
grazing
pressure.
Consistent
with
the
latter
hypothesis,
significantly
more
biomass
of
the
largely
fungivorous
collembola
and
mites
was
found
in
the
top
10cm
of
no-tillage
fallow
dryland
wheat
plots
than
in
stubble
mulched
plots,
whereas no significant
differences in
the
biomass
of
the
largely
bacterivorous
protozoa
and holophagous
nematodes
were
established
(Elliott
et
al.
1984).
Likewise,
Hendrix
et
al. (1986)
found
significantly
higher
numbers
and
bio-
mass
of
fungivorous
nematodes
and
largely
fungivorous
microarthropods
in
the
topsoil
of
a
sandy
clay
loam;
in
this
case
the
bacterivorous
nematodes
were
significantly
lower
in
number and
biomass.
Lower
abundances
of
fungi
and
higher
numbers
of
fungivorous nematodes and
prostigmatid
mites
were
found
in
surface
weed
residues
on
an
upland
site,
suggesting
reduced fungal
popula-
tions
caused
by
grazing,
but
no
such
results
were
found
in
the
same
litter
at
a
lowland
site
(Parmelee
et
al.
1989).
In
conclusion,
there
is
circumstantial
evidence
for
the
quantitative
impor-
tance
of
the fungal
energy
channel including
the
fungivorous
fauna
for
decom-
position and mineralization
in
no-tillage
or
reduced
tillage
agriculture.
7.
Research
needs
Dynamic
models
The
use
of
simulation
modelling
is
indispensable for
the
description, prediction
and,
ultimately,
the
application
in
management
of
the
contribution
of
the
soil
biota
to
element
turnover
in
soil.
The
approach
we
have
chosen
in
this
article
relies
heavily
on
the
applicability
of
food
web
models
such
as
the
one
by
Hunt
et
al. (1987;
Fig.
5).
Although
this
model
appears
to
be
the
best available
for
the
description
of
faunal
influence
on
decomposition
and
mineralization,
several

202
Log
number
100
g'soil
4
3.5
3
2.5
2
10
-3)
10
-
1)
0 3 6
Time
(weeks)
Fig.
18.
Population
growth
of
the
bacterivorous nematode
Rhabditis
sp.
at
100
C
in
the
absence
and
at
various
inoculum
densities
of
the
nematophagous
fungus
Arthrobotrys
sp.
(:1,
I
x 10-,
I
x
10-2
,
1
x
10- 3
,
0)
in
a
microcosm
experiment.
(From
Bouwman
et
al.
in
prep.).
limitations
have
to
be
kept
in
mind.
The
basic
assumption
is
that
the
functional
groups
process
energy
and nutrients
by
digestion
of
food
and
through
their
own
population
turnover.
However,
top
predators
not
only
process
matter,
but
can
also
impact
the
abundance and
amount
of
energy
and nutrients
processed
by
prey,
even
though
they
have
a relatively
low
biomass
compared
with
the
lower
trophic
groups.
One may argue
that
these
effects
are
accounted
for
by
the
model
in
the
biomass
and
the
turnover
of
the
lower
trophic
level
groups,
but
our point
is
that
the
higher
animals
are more
important
than
is
apparent
from
the
amount
of matter
processed
by
them.
Moore
et
al.
(1988)
estimated from
the
model
of
Hunt
et
al.
(1987)
what fraction
of
the secondary
production
of
each
functional
group
went
to
consumers.
The
fraction
ranged
from
1-4%
in
protozoa,
0-11%
in
microarthropods,
10-52% in
nematodes
and
just
over
30%
in
bacteria
and
fungi.
Among
the
predators
a
strong regulation
potential
on
bacteria
was
calculated
for predatory
nematodes
and
mites
and
on
fungi
for
predatory
mites.
The
second
limitation to
be
considered
is
that
any
effects
of
pathogens
and
parasites
on
abundance
and
activity
of
the
functional groups
are
not
accounted
for
in the
trophic
relationships.
The
effect
of
the
presence
of
predatory
fungi
on
the
population
growth
of
bacterivorous
nematodes
was
measured
in
micro-
cosms
to
which
pulverized beet
leaves
were
added
in
amounts
equivalent
to
those normally
applied
to
the
field
soil
in
autumn
(Bouwman
et
al.
in
prep.).
After
a
treatment
of
y-irradiation
(1
Mrad)
which
was
followed by
addition
of
a
suspension
of
bacteria
and
nematodes,
the
nematode-trapping
fungus
Arthro-
botrys
sp. was
able
to
reduce
the
numbers
of
the
nematodes
Rhabditis
sp.
(Fig.
18)
and
Acrobeloides
sp.
depending
on
the
inoculum
density
of
the fungus.
The

203
same
held
for
the
nematode-trapping
fungus
Dactylaria
sp.
versus
Rhabditis
sp.
and
to
a
lesser
extent
versus
Acrobeloides.
The
third
limitation
of
the
model
is
that
the
saprophagous
fauna
is
not
included.
Sensitivity
analysis showed
that
reliable
information
about
population
sizes,
population
turnover
rates,
C/N
ratio
of
fauna,
digestibility
of
prey
and
P/A
ratio
is
necessary
to
successfully
apply
this
model
(Hunt
et
al.
1987).
There
is
an
urgent
need
for
more
reliable
estimates
of
ecophysiological
and
population
biological
parameters
of
the
most
important
representatives
of
the
functional
groups,
i.e.
of
the
most
numerous and
metabolically
most
active
species.
Fur-
thermore,
nitrogen
mineralization during
the
growing season
was
modelled
by
Hunt
et
al.
(1987)
to
occur
during
40
ideal
days when the
system
was
considered
in
steady state. Evidently,
this
is
a
justified
first
approximation.
Yet,
accounting
for
short-term
changes
is
necessary
for the
model
to
be
applicable
under
pertur-
bation
conditions.
Recently
Hunt
et
al.
(1989)
developed
a
more dynamic model
for
estimating
components
of
secondary
production
in
the
detrital food
webs
of
a
native
short-
grass
steppe,
winter wheat
and
fallow
plots
after
wetting.
This model
has
been
fitted
to observed
net
changes
in
biomass
and
has been
constrained to
use
transfer
rates compatible
with
the
physiology
and
population
attributes
of
the
organisms. The
authors
found
high
agreement
between
predicted
and
observed
net
changes
in
biomass
and
CO
2
evolution.
However,
the
model
failed
to
account
for
data
with
the
same
parameter
values
across
data
sets
(as
time
and
location).
Therefore,
a
more
mechanistic
model
including
effects
of
the environ-
ment
on
organism
activity
is
to
be
developed.
Perturbation
in
relation
to
microbial
dominance
Several
examples
have
been
given
of
nutrient
leaks
following
perturbation
and
coinciding
with
fewer
soil
animals,
which
also
show
a
shift
in
their
seasonal
abundance
as
compared
with
natural
conditions.
Also,
several
studies
were
referred to,
in
which
the
soil
fauna
was
shown
to
mitigate
the
effects
of
changes
in
abiotic
conditions,
notably
soil
moisture,
so
that
mineralization
of
nitrogen
continued
for
some time
as
stress
developed.
It
is
a
provoking
thought
that
under
those
conditions
mineral
nitrogen
would accumulate,
being
immediately
available
for
plant uptake
upon
rewetting
of
the
soil.
Other
studies
showed
that
immediately
thereafter the
fauna
is
also
important
in
grazing
the
rapidly
in-
creased
microbiota,
thereby again
making nitrogen
available
to
the
plant.
Some
evidence
was
referred
to,
that
also
on
a
seasonal
scale
the
fauna under
natural
conditions
is
instrumental
in
supplying the
plant
with
nitrogen
when
it
needs
it
and
in
preventing
nitrogen
loss
when
there
is
no
plant
demand.
This
hypothesis
warrants
careful
study
because
the answer
may
have
important
implications
for
the
degree
and
the timing
of
man-imposed
perturbations
since
we
aim
at
improvement
of
the
nutrient
use
efficiency
in
agriculture
and
forestry.

204
Fig.
19.
Conceptual
model
of
detritus
food
web
in
fungal
dominated
no-till
systems
(I)
and
bacterial
dominated
conventional
tillage
systems (II).
For
description
of
symbols
see
Fig.
6.
(After
Hendrix
et
al.
1986).
Conceptual
models
of
detritus
food
webs,
being
relatively
more
fungal
domi-
nated
in
no-till
systems
and
bacterial
dominated
in
conventional
tillage systems
(Hendrix
et
al.
1986;
Fig.
19)
can
be
a
useful
framework
for
further
research.
These
conceptual
models
are
being
tested
also
for
nutrient
poor
coniferous
forest
floors
and
those
subjected
to increased
nitrogen deposition,
the
hypothe-
sis
being
that
they show
more fungal
and
bacterial
dominated
nutrient
path-
ways,
respectively
(Verhoef
et
al.
1989).
In the
absence
of
concurrently
collected
data
on microbial
and
faunal
biomass
and
activity the
question
whether
the fungal
biomass
in
no-tillage
and
reduced
tillage
agro-ecosystems
can
support
a
fungivorous
fauna
that
is
able to
influence
or
even
regulate
the
standing
stock
of
fungi
with
quantitatively
important
effects
on the
decomposition
of
organic
matter
and
the
mineralization
of
nutrients,
is
still
open for
research.
Experiments with
litterbags
with
various
mesh-sizes,
extending
the research
of
Holland
&
Coleman
(1987)
to
include the
soil
fauna
seem
to
be
promising
in
this
respect.
Similar
experiments with forest
litter under
conditions
of
low
and
high
aerial
deposition
of
nitrogen
are
performed
in
current
research
in the
Netherlands
(Verhoef et
al.
in
prep.).

205
In studying
nutrient
pathways
through
the
fauna
in supposedly fungal domi-
nated
no-tillage
and
bacterial
dominated
conventional
tillage
systems,
differen-
ces
in
soil
structure
between
these
systems
should
be
taken
into
account.
Small,
lower
trophic
level
animals
living in
water-filled
pores
or
water
films
may
make
more
food
available
to
bigger,
higher
trophic
level
animals
by
entering
soil
pores
inaccessible
to the
latter.
Evidence
therefore
was
found
for
amoebae
emerging
from
small
pores
and
subsequently
eaten
by
nematodes
that
were
unable
to
enter
those pores
(Elliott
et
al.
1980).
Also,
microarthropods
living
in
the
air-filled
pores
will
be
largely
restricted
in
their grazing
and
predatory
activities
to
interconnected pores
exceeding
certain
diameters
in neck
size.
On the
other
hand, although
no-tillage
soil
may
have
a
higher bulk
density (Westmaas
Research
Group
on New
Tillage Systems
1984),
a
greater
proportion
of
pores
and
channels can
be
formed
by
the
soil
biota,
i.e.
roots
and fauna
(Kooistra
et
al.
1989;
Fig.
20),
while
the
fauna
also
mixes
crop
residues
with mineral
soil.
To
what
extent
these
processes
interact
to
yield
the
contributions
of
various
func-
tional
groups
of
soil
fauna
to
organic
matter
dynamics (decomposition
and
humification)
and
nutrient
mobilization
seems
to
be
a
research
area
hardly
touched
upon
hitherto.
Ecological applications
and
ecological
theory
In
this
paper
we
stressed
the
need
to
further
test
the
hypothesis
that
different
assemblages
of
species
with
a
common
resource
base,
i.e.
energy
channels,
are
important
during
decomposition
of
organic
matter
and
mineralization
of
nu-
trients.
We
also
put
forward
the
hypothesis
that
the
nutrient
supply
from
the
soil
and
the
uptake
by
the
plants
are
better
synchronized
and
synlocalized
under
natural
conditions
than
under
perturbation.
If
these
hypotheses
are
true
the
implications for
forestry and agriculture
are
clear:
the
energy
channels
and
nutrient
pathways
should
be
manipulated towards retention
of
organic
matter
where
needed
and reduction
of
nutrient
leakage
where
possible.
A
recent
revival in
the discussions
on
ecological
theories
on
food
webs
is
apparent
(Schoener
1989;
Briand
&
Cohen
1987;
Moore
&
Hunt
1988).
Schoener
(1989)
states
in
his
thorough
review
that
there
is
few
integration
between
the three
levels
at
which
trophic
ecology
can
be
conceptualized:
the
individual,
population
and
community
level.
At
the
population
level
the
stable
dynamical
theory
(review
in
Pimm
1982)
has
proved
its
worth
to explain
specific
food
web
phenomena,
such
as
the
destabilizing
effects
of
feeding
on
more
than
one
trophic
level
(Pimm &
Lawton
1978).
However,
it
fails
to
link
individual-
level
concepts
to
food
web
patterns.
The
community
level
approach
of
Cohen
et
al. (1985)
hardly
draws on
lower
level
concepts.
According
to
Schoener
(1989)
a
more
reductionist
approach
would
help
to
unify the
different
theoretical
levels.
Partly
based
on
his
own
studies
on
a
simple
terrestrial
food
web
on Bahamian
islands
and
partly
on
an
analysis
of
98
food
webs
compiled
by
Briand
&
Cohen
(1987),
Schoener
(1989)
proposes
the
'productive
space'
hypothesis.
It
states
that
maximum
food chain
lengths
are
determined
by
the
amount
of
productive

206
Conventional
tillage
total
20
40
60
80 100%
macroporosity
,J
ra
10
20
4.1
%
'1
L-
---- ---- -
c2s
Minimum
tiltage
20
1
5.6
%
40
60
80
100%
p1
recent)
,p2
ploughpan)
,p
3
former)
,
-I__ __----------csI v o
i s d e d
b
tillage
voids,
pressure
induced
cracks
idea,
modified
voids
produced
by
soil
organisms,
inc.
roots
natural
cracks
pedal
iE//
11.6
%
2.4/
%
4.8
%
7.6 %
Fig.
20.
Macroporosity
and
origin
of
pores
in
a
conventional
and a
minimum
tillage
arable
cropping
system
on
a
sandy loam
soil.
(From Kooistra
et
al.
1989).
space
(=
space
times
productivity)
required
to
allow
critical
component
species
populations
to persist
with
some
high
probability
(Schoener
1989;
p.
1568).
The
food
webs
concern
above-ground
terrestrial and
aquatic
system categories,
and
show
striking
similarities,
such as
in
the
number
of
trophic
species,
but
also
major
differences
in
food
chain
lengths.
This
latter
conclusion
is
critized
by
Moore
et
al.
(1989)
by
stating
that
many
of
the
food
webs
used
show
consider-
able
incompleteness:
they
are
missing
predatory
birds
and
insects
and
primary
decomposers
such
as
bacteria
and
saprophytic
fungi.
They
suggest
that
the
30
0
L.
3r
E
20
30
C
Ap

207
aquatic
two-dimensional
and
the
terrestrial
three-dimensional
webs
are
descrip-
tions
of
habitat
compartments
of
real
food
webs,
which
is
consistent with the
resource
compartmentation
hypothesis
and
niche
theory.
Yodzis
(1984)
found,
based on
34
webs
of
the
Briand
&
Cohen-collection
(1987)
that
energy
flow
explains
variation
in
food
chain length
better
than
do
limitations
resulting
from
dynamical stability
or
the
body
size
of
predators.
According
to
Briand
&
Cohen
(1989)
the
influence
of
energy
versus
that
of
other
factors
on
food
chain
length
must
be
further
analyzed.
Moore
&
Hunt
(1988)
have
provided
evidence
of
resource
compartmentation
based
on
structural
characteristics
of
a
below-
ground
connectedness
web
and
on
biomass
estimates
and
nitrogen
flux
rates
from
its energy
flux-web
description. According
to
these
authors
analyses
of
the
utilization
of
energy
coupled
with
qualitative
analyses
of
connectedness
webs
are
appropriate
to
reveal
aspects
of
food
web
structure
and
stability. This
below-ground study
concerns
the
earlier
mentioned shortgrass
steppe
food
web
(see
Fig.
5).
Similar
below-ground
studies
are
performed
in
current
research
in
the
Netherlands,
both
in
agro-ecosystems
and
pine
forests.
We
feel
that
the
hypotheses
on
energy
channels,
nutrient
pathways
and
synchronization
and
synlocalization
both
should
dwell
on
recent
developments
in
ecological
theory
and
contribute
to
it,
because
it
is
only
on a
sound
theoretical
basis
that
ecologi-
cal
knowledge
of
the
soil
fauna
can
be
applied to
the
management
of
element
transfer
in
forestry
and
agriculture.
Acknowledgements
The
authors
thank
drs
J.C. Moore, H.W.
Hunt
(Natural
Resource Ecology
Laboratory,
Fort
Collins,
Colorado,
U.S.A.),
dr.
O.
Andren
(Department of
Ecology
and
Environmental
Research,
Uppsala,
Sweden)
and
an
anonymous
reviewer
for
constructive comments
during
the
preparation
of
the
manuscript.
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