Reducing tillage in cultivated fields increases earthworm functional diversity

Abstract

Alternative cropping systems such as conservation agriculture have been implemented to limit the harmful effects of intensive conventional cropping systems. Conservation agriculture is known to modify the structural diversity of earthworm communities, but no data have been reported so far on their functional diversity. Structural and functional indices of community were used to study the effects of different soil tillage intensity on earthworm diversity in arable soils.

Field data were collected in four agricultural trials across France representing different soiland climatic conditions. Three types of soil tillage were assessed: plowing, superficial tillage and direct seeding. Earthworm abundance, species richness and ecomorphological group abundance were investigated. Seven functional traits, i.e. body length, body mass/length ratio, epithelium type, cocoon diameter, typhlosolis type, carbon preferences and vertical distribution, were selected according to their hypothesized link with mechanisms of tillage impact. Functional diversity indices were then computed. Soil tillage intensity decreased functional diversity and modified the functional trait profile within the earthworm community whereas neither structural diversity (species number) nor abundance changed with tillage intensity. Differences between plowing and direct seeding were significant in each trial, and superficial tillage often showed intermediate trait values. Regarding ecomorphological groups, anecic abundance was positively influenced by a decrease in soil tillage, contrary to epigeic and endogeic earthworms that showed no response. Tillage acts as an environmental filter, and decreasing its intensity caused a lesser convergence of traits and thus higher functional trait diversity. We demonstrated that a trait-based approach better permitted comparisons of community responses across sites than species number or abundance.

Full text

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
Applied
Soil
Ecology
xxx (2013) xxx–
xxx
Contents
lists
available
at
ScienceDirect
Applied
Soil
Ecology
journal
h
om
epage:
www.elsevier.com/locate/apsoil
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity
C.
Pelosia,∗,
B.
Peya,b,
M.
Heddea,
G.
Caroa,
Y.
Capowiezc,
M.
Guerniond,
J.
Peignée,
D.
Pirond,
M.
Bertrandf,g,
D.
Cluzeaud
aINRA,
UR251
PESSAC,
F-78026
Versailles
Cedex,
France
bCESAB/FRB,
Domaine
du
Petit
Arbois,
Avenue
Louis
Philibert,
F-13545
Aix-en-Provence,
France
cINRA,
UR1115
Plantes
et
Systèmes
Horticoles,
Site
Agroparc,
F-84914
Avignon
Cedex
09,
France
dUMR
6553
EcoBio,
Univ-Rennes
1,
CNRS,
Station
Biologique,
F-35380
Paimpont,
France
eISARA
Lyon/Université
de
Lyon,
23
rue
Jean
Baldassini,
F-69007
Lyon,
France
fINRA,
UMR211
Agronomie,
F-78850
Thiverval-Grignon,
France
gAgroParisTech,
UMR211
Agronomie,
F-78850
Thiverval-Grignon,
France
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
2
February
2013
Received
in
revised
form
10
October
2013
Accepted
20
October
2013
Keywords:
Earthworms
Functional
traits
Plowing
Direct
seeding
Tillage
Soil
a
b
s
t
r
a
c
t
Alternative
cropping
systems
such
as
conservation
agriculture
have
been
implemented
to
limit
the
harm-
ful
effects
of
intensive
conventional
cropping
systems.
Conservation
agriculture
is
known
to
modify
the
structural
diversity
of
earthworm
communities,
but
no
data
have
been
reported
so
far
on
their
functional
diversity.
Structural
and
functional
indices
of
community
were
used
to
study
the
effects
of
different
soil
tillage
intensity
on
earthworm
diversity
in
arable
soils.
Field
data
were
collected
in
four
agricultural
trials
across
France
representing
different
soiland
climatic
conditions.
Three
types
of
soil
tillage
were
assessed:
plowing,
superficial
tillage
and
direct
seeding.
Earth-
worm
abundance,
species
richness
and
ecomorphological
group
abundance
were
investigated.
Seven
functional
traits,
i.e.
body
length,
body
mass/length
ratio,
epithelium
type,
cocoon
diameter,
typhloso-
lis
type,
carbon
preferences
and
vertical
distribution,
were
selected
according
to
their
hypothesized
link
with
mechanisms
of
tillage
impact.
Functional
diversity
indices
were
then
computed.
Soil
tillage
intensity
decreased
functional
diversity
and
modified
the
functional
trait
profile
within
the
earthworm
commu-
nity
whereas
neither
structural
diversity
(species
number)
nor
abundance
changed
with
tillage
intensity.
Differences
between
plowing
and
direct
seeding
were
significant
in
each
trial,
and
superficial
tillage
often
showed
intermediate
trait
values.
Regarding
ecomorphological
groups,
anecic
abundance
was
positively
influenced
by
a
decrease
in
soil
tillage,
contrary
to
epigeic
and
endogeic
earthworms
that
showed
no
response.
Tillage
acts
as
an
environmental
filter,
and
decreasing
its
intensity
caused
a
lesser
convergence
of
traits
and
thus
higher
functional
trait
diversity.
We
demonstrated
that
a
trait-based
approach
better
permitted
comparisons
of
community
responses
across
sites
than
species
number
or
abundance.
© 2013 Elsevier B.V. All rights reserved.
1.
Introduction
Agricultural
intensification
has
reduced
soil
biodiversity
in
cul-
tivated
fields.
Many
authors
have
reported
negative
impacts
of
plowing,
pesticide
use,
simplification
of
crop
rotations
and
land
use
management
on
several
soil
invertebrate
communities
(Bengtsson
et
al.,
2005;
Hubbard
et
al.,
1999;
Doran
and
Zeiss,
2000).
Earth-
worms,
which
represent
a
large
proportion
of
soil
biomass,
i.e.
up
to
80%
(Yasmin
and
D’Souza,
2010),
are
highly
sensitive
to
soil
tillage
(Chan,
2001;
Hubbard
et
al.,
1999).
They
have
important
agro-
ecological
functions
(Edwards
and
Bohlen,
1996;
Sims
and
Gerard,
∗Corresponding
author
at:
UR251
PESSAC,
INRA,
Bâtiment
6,
RD
10,
F-78026
Versailles
Cedex,
France.
Tel.:
+33
1
30
83
36
07;
fax:
+33
1
30
83
32
59.
E-mail
address:
celine.pelosi@versailles.inra.fr
(C.
Pelosi).
1999)
and
are
well-known
ecosystem
engineers
(Jones
et
al.,
1994)
and
bioindicators
of
soil
biological
functioning
(Paoletti,
1999).
Reduced
or
non-inversion
tillage
cropping
systems
are
thought
to
be
beneficial
to
these
soil
organisms
(Bengtsson
et
al.,
2005;
Pelosi
et
al.,
2009).
Among
them,
conservation
agriculture
was
first
proposed
to
limit
soil
erosion
and
thus
ensure
the
sustain-
ability
of
some
farming
systems.
It
combines
minimum
tillage,
diversified
crop
rotations
and
permanent
cover
crops
to
manage
weeds
and
pests
and
to
reduce
erosion
(FAO).
The
development
of
these
alternative
cropping
systems,
with
reduced
mechanical
dis-
turbance,
influences
earthworm
community
structure
(Fonte
et
al.,
2009;
Pelosi
et
al.,
2009)
and
thus
the
associated
ecological
services
(Capowiez
et
al.,
2009).
Functional
diversity
of
a
community
can
be
measured
by
several
approaches
(Bernhardt-Röermann
et
al.,
2008),
including
(i)
the
diversity
of
a
priori
functional
groups,
(ii)
the
diversity
of
0929-1393/$
–
see
front
matter ©
2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.apsoil.2013.10.005

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
2C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx
mathematically
determined
functional
groups,
and
(iii)
synthetic
indices
based
on
functional
traits.
Functional
trait
concepts
have
emerged
as
a
promising
way
for
understanding
the
mechanisms
that
drive
organism
responses
to
environmental
disturbances
(e.g.
the
habitat
templet
theory;
Southwood,
1977).
Functional
traits
concern
species
properties
that
affect
individual
fitness
and
govern
species’
responses
to
their
environment
(Violle
et
al.,
2007).
Trait-
based
approaches
are
currently
used
in
different
fields
of
ecology,
e.g.
plant
or
stream
invertebrate
ecology
(Archaimbault
et
al.,
2010;
Lavorel
and
Garnier,
2002).
They
have
been
less
studied
in
soil
ecology,
although
functional
trait
profiles
have
been
stressed
to
be
a
consistent
way
to
reveal
earthworm
responses
to
environ-
mental
perturbations
(Fournier
et
al.,
2012;
Hedde
et
al.,
2012;
Pérès
et
al.,
2011).
Traits
have
to
be
selected
for
their
perceived
relevance
to
tested
environmental
drivers.
Ideally,
considerations
of
biological
and
ecological
functions
would
be
related
directly
to
purely
functional
traits
such
as
growth,
reproduction,
and
competitive
ability.
However,
direct
measurements
of
biological
and
ecological
properties
and
processes
are
often
impractical.
We
therefore
focused
on
easily
measured
or
well-known
features
that
may
act
as
surrogates
for
such
properties
and
processes.
Morpho-
logical
traits
can
be
surrogates
for
growth/maintenance
(e.g.
body
length,
body
mass/length
ratio,
presence/size
of
a
typhlosolis,
i.e.
a
mid-dorsal
invagination
of
the
earthworm
midgut
that
may
be
involved
in
nutrient
uptake
efficiency,
Stevens
and
Hume,
1995),
protection
(e.g.
epithelium
type)
or
investment
in
reproduction
(e.g.
cocoon
diameter).
Behavioral
traits,
like
earthworm
species’
vertical
distribution,
may
also
reflect
the
response
of
individuals,
notably
in
term
of
exposure
to
disturbance.
Finally,
ecological
preference
like
carbon
content
preferences
can
also
be
used
to
test
earthworm
responses
to
modification
in
soil
properties
and
functioning
(in
terms
e.g.
of
pH
or
organic
matter
content).
Up
to
now,
earthworm
functional
diversity
has
been
charac-
terized
using
a
priori
functional
groups,
i.e.
the
ecomorphological
groups
defined
by
Bouché
(1972).
Anecics
are
generally
less
abun-
dant
or
even
absent
in
plowed
fields
(Chan,
2001).
The
direct
(mechanical
damage
and
exposure
to
predation)
or
the
indirect
deleterious
impacts
of
plowing
(changes
in
soil
environment,
including
destruction
of
burrows,
burying
of
surface
organic
mat-
ter
and
changes
in
soil
physical
conditions
such
as
water
content
and
temperature)
may
explain
these
results
(Chan,
2001;
Edwards
and
Bohlen,
1996).
The
lack
of
an
organic
layer
in
plowed
systems
strongly
constrains
the
survival
of
epigeic
species
in
these
systems.
The
endogeic
species,
living
in
the
top
20
cm
of
soil,
may
be
reduced
(De
Oliveira
et
al.,
2012)
or
favored
by
plowing
(Nuutinen,
1992;
Pelosi
et
al.,
2009;
Wyss
and
Glasstetter,
1992)
since
they
could
take
advantage
of
crop
residues
in
the
soil
made
available
to
them
through
incorporation
(Chan,
2001).
The
present
work
aims
at
studying
the
effects
of
different
soil
mechanical
disturbances
on
earthworm
communities
in
arable
soils.
We
used
data
from
several
trials
testing
different
types
of
tillage,
i.e.
plowing,
superficial
tillage,
and
direct
seeding.
To
estab-
lish
the
generality
of
results
(soil
and
climate
independency),
data
were
collected
in
agricultural
trials
in
four
sites
across
France.
We
tested
the
effect
of
a
decrease
of
tillage
intensity
on
different
descriptors
of
earthworm
communities
(total
abundance,
species
richness,
ecomorphological
group
abundance
and
functional
trait
diversity)
and
compared
them.
We
hypothesized
that
a
decrease
in
soil
tillage
leads
to
an
increase
of
the
carrying
capacity
of
soil
(earth-
worm
density),
of
species
richness
and
of
functional
trait
diversity
due
to
less
harsh
conditions.
First,
concerning
ecomorphological
groups,
we
hypothesized
that
(1)
mechanical
de-intensification
changes
their
distribution,
favoring
anecics,
as
well
as
the
species
living
in
the
topsoil,
mostly
epigeics,
due
to
the
progressive
establishment
of
an
organic
layer.
Second,
tillage
acts
as
an
envi-
ronmental
filter,
hence
(2)
functional
traits
converge
to
a
narrower
range
of
values
with
increasing
of
intensity
of
tillage.
Regarding
the
diversity
of
traits,
four
sub-hypotheses
are
considered:
(3.1)
the
largest
and
the
most
fragile
(with
a
supple
epithelium)
organ-
isms
are
most
affected
by
intensive
tillage.
(3.2)
More
earthworms
with
a
larger
feather
typhlosolis
are
found
in
plots
with
lower
nutri-
ent
availability,
i.e.
the
plowed
plots.
This
hypothesis
is
based
on
Stevens
and
Hume
(1995)
who
found
that
a
larger
feather
typhloso-
lis
is
associated
with
higher
nutrient
uptake
efficiency.
(3.3)
As
a
consequence,
a
higher
proportion
of
earthworms
with
high
soil
car-
bon
content
requirement
is
found
in
unplowed
plots.
Finally,
(3.4)
the
more
an
individual
lives
in
the
topsoil,
the
more
it
suffers
from
plowing.
2.
Materials
and
methods
2.1.
Sites
and
cropping
systems
Field
data
were
collected
from
agricultural
trials
in
four
differ-
ent
localities
in
France
(Table
1).
According
to
the
FAO
classification,
soils
were
Cambisol
on
trial
A,
Luvisols
on
trials
B
and
C,
and
Fluvisol
on
trial
D.
Climatic
conditions
are
temperate
and
presented
a
vari-
able
oceanic
influence,
from
oceanic
(trial
A–C)
to
continental
(trial
D)
climates
(Table
1).
Trials
compared
at
least
two
different
types
of
soil
tillage:
plowing,
superficial
tillage
and
direct
seeding
(Table
2).
Plowing
involved
soil
inversion
to
25–30
cm
depth.
Superficial
tillage
involved
mechanical
disturbance
to
less
than
8
cm
depth,
without
soil
inversion.
Direct
seeding
involved
mechanical
distur-
bance
in
the
upper
3
cm
of
soil
in
the
sowing
furrows,
without
soil
inversion.
The
number
of
replicated
plots
per
tillage
type
in
each
individual
trial
was
6
for
trial
A,
2
for
trial
B,
3
for
trial
C,
2
or
3
for
trial
D.
Information
on
crop
rotations,
pesticide
use
and
fertilization
is
given
in
Table
2.
Physico-chemical
characteristics
of
soils
are
detailed
in
Table
1.
Soils
were
loamy
(trials
B
and
C)
to
sandy
(trial
D)
textured.
Soil
texture
differed
between
tillage
type
within
trial
C
and,
to
a
lesser
extent,
trial
D.
Soil
pH
values
were
associated
with
bedrocks,
from
granite
in
trial
A
(pH–H2O
=
6.2)
to
aerial
loess
deposits
in
trials
B
and
C
(pH–H2O
=
7.0–7.6)
and
carbonated
alluvium
deposits
in
trial
D
(pH–H2O
=
7.8–7.9).
Similarly,
CaCO3content
reflected
the
bedrock
nature
of
each
site
but
no
differences
existed
within
plots
of
the
same
site.
Organic
matter
content
was
higher
in
soils
of
trial
A
than
in
the
other
soils
(35
and
14–21
g
kg−1respectively).
No
differ-
ences
occurred
between
tillage
types
in
trial
A
whereas
soil
organic
matter
content
was
increased
when
conservation
agriculture
had
been
adopted
in
the
other
three
trials.
The
gain
ranged
from
+6%
to
+25%
in
trial
D
(plowing
vs
surface
tillage)
and
B
(plowing
vs
direct
seeding)
respectively.
2.2.
Earthworm
sampling
methods
The
main
characteristics
of
the
sampling
design
of
each
study
are
given
in
Table
3.
All
studies
were
carried
out
during
autumn
(November)
or
early
spring
(March–April),
when
most
earthworm
species
are
particularly
active
(Bouché,
1972).
Samplings
were
mostly
done
on
winter
wheat
crops,
but
some
were
done
on
flax
or
sugar
beet
(trial
C)
and
on
soybean
residues
or
wheat/alfalfa
crop
associations
(trial
D).
In
all
the
trials,
the
sampling
method
combined
chemical
extraction
(using
different
chemicals)
and
hand-sorting
(Table
3).
The
number
of
replicates
per
plot
was
2
in
trial
D,
3
in
trial
A,
4
in
trial
C
and
5
in
trial
B.
Depending
on
the
trial,
sampling
was
done
from
1995
to
2011.
As
the
number
of
years
since
the
trial
establishment
ranged
from
3
to
14,
and
because
of
the
year-to-year
weather
variation,
we
incorporated
the
between-
year
differences
by
computing
median
values
of
earthworm
species
densities
at
the
plot
level.
Despite
differences
in
sampling
design

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx 3
Table
1
Soil
and
climatic
characteristics
of
the
four
agricultural
trials.
DS,
ST
and
P
refer
to
direct
seeding,
superficial
tillage,
and
plowing,
respectively.
Site
name
Trial
A:
Kerguehennec
Trial
B:
Versailles
Trial
C:
Mons
Trial
D:
Thil
Localization
47◦52N,
02◦46W
48◦48N,
2◦08E
45◦49N,
5◦20E
Climatic
conditions:
Mean
annual
temperature
(◦C) 11.5
10.4
9.6
11.4
Mean
annual
precipitation
(mm)
890
640
667
830
Tillage
type
DS
ST
P
DS
P
ST
P
DS
ST
P
Soil
characterization
(0–25
cm
depth)
Sand
(g
kg−1)
425.0
399.0
392.0
305.5
215.5
191.0
235.0
609.0
576.0
562.0
Silt
(g
kg−1)
413.0
437.0
442.0
531.0
629.8
759.0
665.0
256.0
271.0
266.0
Clay
(g
kg−1) 162.0 164.0 166.0 163.8 179.5 50.0 93.0
135.0
152.0
171.0
Organic
matter
(g
kg−1) 35.4 35.3 35.0 21.7 17.3 17.1
14.0
17.9
16.5
15.6
C/N
ratio 10.7
11.3
11.1
11.2
10.6
10.1
10.2
8.8
9.1
8.9
pH–H2O
6.2
6.2
6.2
7.0
7.4
7.6
7.5
7.8
7.9
7.8
CaCO3(g
kg−1)
<1
<1
<1
<1
<1
5.0
5.0
218.0
225.0
221.0
CEC
9.2
9.1
9.4
9.1
9.7
9.1
9.3
5.7
5.7
5.7
Soil
type
(FAO
classification)
Cambisol
Luvisol
Luvisol
Fluvisol
Table
2
Crop
management
in
the
four
agricultural
trials.
Site
name
Crop
rotation
Soil
tillage
Pesticide
use
Fertilization
A
(Kerguehennec)
Maize,
wheat,
rape,
wheat Direct
seeding
Conventional
Mineral
Superficial
Tillage
Plowing
B
(Versailles) Pea,
wheat,
maize,
wheat
Direct
seeding Conventional
Mineral
Oilseed
rape,
wheat,
pea,
wheat
Plowing
C
(Mons) Sugarbeet,
wheat,
maize,
wheat
Superficial
Tillage Conventional
Mineral
Plowing
D
(Thil)
Alfalfa,
maize/oat,
soybean,
wheat/rye,
soybean,
wheat/alfalfa
Direct
seeding
No Organic
or
none
Superficial
Tillage
Plowing
(both
in
time
and
space),
aggregating
earthworm
densities
at
plot
level
gives
a
reliable
picture
of
species
composition
and
densities
of
local
communities.
Such
an
aggregation
has
already
been
used
by
Decaëns
et
al.
(2008)
to
test
for
assembly
rules
within
earthworm
communities
at
regional
scale,
with
results
coming
from
different
sampling
protocols
in
terms
of
methods
of
extraction,
number
of
fields
per
habitat
and
of
replicates
per
field
or
distance
between
replicates.
2.3.
Earthworm
functional
traits
Seven
traits
were
selected
for
their
perceived
relevance
to
tillage
effect,
five
being
morphological
(i.e.
body
length,
body
mass/length
ratio,
epithelium
type,
cocoon
diameter
and
typhlosolis
shape),
one
each
being
behavioral
(i.e.
vertical
distribution
within
soil)
and
ecological
(i.e.
carbon
requirement).
Morphological
and
ecologi-
cal
traits
were
obtained
from
Bouché
(1972)
and
Sims
and
Gerard
(1999).
The
latter
reference
was
used
for
morphological
traits
only.
Bouché
(1972)
gives
Corg
values
for
each
earthworm
sampling
point.
We
estimated
the
C
requirements
of
species
according
to
their
frequency
distribution
on
the
Corg
gradient.
Earthworm
ver-
tical
distribution
was
based
on
the
authors’
expertise
and
literature
data
(Gerard,
1967;
Lavelle,
1998;
Rundgren,
1975).
There
are
several
approaches
to
deal
with
trait
data,
e.g.
work-
ing
with
species
maximum
or
median
trait
values
(Ribera
et
al.,
2001),
by
establishing
the
probability
distribution
over
different
classes
of
a
trait
(Chevenet
et
al.,
1994;
Hedde
et
al.,
2012;
De
Lange
et
al.,
2013)
or
by
multivariate
analyses
(De
Lange
et
al.,
2013).
As
mentioned
by
Statzner
et
al.
(1994),
using
specific
numerical
val-
ues
is
not
really
appropriate
because
of
the
variability
of
values
observed
for
a
species.
Rather,
fuzzy
coding
can
describe
the
affin-
ity
of
a
species
for
different
attributes
(i.e.
classes)
of
a
trait
and
is
now
widely
used
in
aquatic
ecology
(Chevenet
et
al.,
1994).
We
followed
the
procedure
described
by
Hedde
et
al.
(2012).
Briefly,
Table
3
Earthworm
sampling
methods
in
the
four
agricultural
trials.
Site
name
Number
of
years
since
trial
establishment
Sampling
period
Sampling
method
Reference
for
the
method
Size
of
sampling
unit
(m2)
Number
of
replicates/system
Number
of
points/replicate
A
(Kerguehennec)
7
years
Spring
Formalin,
hand-sorting
Cluzeau
et
al.
(1999)
1
3
3
B
(Versailles)
8,
9,
10,
14
years
Autumn
AITC,
hand-sorting
Pelosi
et
al.
(2009)
0.16
2
5
C
(Mons)
4,
5,
6,
7
years
Autumn
Commercial
mustard,
hand-sorting
Capowiez
et
al.
(2009)
0.16
2
4
D
(Thil)
3,
4,
5
years
Autumn
Formalin,
hand-sorting
Peigné
et
al.
(2009)
1
2
or
3
(at
5
years)
1
or
2
(at
5
years)

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
4C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx
information
was
coded
by
an
affinity
score
ranging
from
0
to
3
for
each
trait
class,
and
affinities
were
summed
to
build
the
trait
profile
(e.g.
the
distribution
of
affinities
within
classes).
Trait
profiles
were
standardized
so
that
their
sum
for
a
given
taxon
and
a
given
trait
equaled
100%.
The
list
of
functional
traits
for
the
different
species
is
presented
in
Appendix
1.
2.4.
Community
parameters
and
associated
statistical
analyses
We
assessed
the
abundance
as
well
as
structural
and
functional
diversities
of
earthworm
communities
for
each
individual
plot.
Earthworm
abundance
was
expressed
as
the
number
of
individ-
uals
per
m2.
We
used
species
richness,
which
was
the
number
of
identified
species,
as
a
measure
of
structural
diversity.
Func-
tional
diversity
was
estimated
by
three
approaches:
(i)
gathering
earthworm
abundances
into
Bouché’s
eco-morphological
groups
(anecic,
endogeic,
epigeic
earthworms),
(ii)
estimating
functional
trait
profiles
calculating
community-weighted
means
(CWM)
of
each
trait
and
(iii)
computing
a
synthetic
index
of
functional
diver-
sity
(the
Rao’s
quadratic
entropy,
RaoQ).
The
CWM,
defined
by
Lavorel
et
al.
(2008)
as
the
weighted
mean
of
trait
classes
in
communities,
was
calculated
using
the
following
formula:
CWM
=
n
pi×
traiti(1)
where
p
is
the
relative
contribution
of
species
i
to
the
community
and
traitiis
the
value
of
the
considered
trait
class
for
species
i.
RaoQ
is
a
suitable
measure
of
functional
diversity
if
several
traits
are
considered.
It
incorporates
both
the
relative
abundances
of
species
and
a
measure
of
the
pairwise
functional
differences
between
species
(Botta-Dukat,
2005).
It
was
calculated
using
the
following
formula
(Botta-Dukat,
2005;
Schleuter
et
al.,
2010):

s
∈
Sc

s∈
Sc
AsAs
A2dist(s,
s)
(2)
where
s
and
sare
two
taxa,
Scis
the
set
of
species
present
in
com-
munity
c,
Asand
Asare
the
respective
abundances
of
the
taxa
s
and
s,
A
is
the
total
abundance
of
all
individuals
and
dist(s,
s)
is
the
distance
between
taxa
pairs,
based
on
mean
trait
class
values
(for
continuous
variables,
Euclidean
distance
is
used;
for
discrete
variables,
the
Gower
distance
is
used).
After
such
a
standardiza-
tion,
RaoQ
values
range
from
0
to
1
and
a
RaoQ
equal
to
1
means
a
maximum
functional
dissimilarity
within
a
community.
Difference
in
species
richness,
earthworm
abundance
and
RaoQ
between
tillage
types
in
each
trial
were
tested
using
non-parametric
tests
(i.e.
Wilcoxon
or
Kruskal–Wallis)
fol-
lowed
by
a
non-parametric
post
hoc
when
significant
(Siegel
and
Castellan,
1988).
Regarding
CWM,
confidence
intervals
(mean
±
0.975
×
standard
deviation)
were
estimated
for
each
trait
class,
and
differences
between
tillage
types
were
considered
to
be
consistent
if
confidence
intervals
did
not
overlap.
All
statis-
tical
analyses
were
performed
with
the
R
statistical
software
(R
Development
Core
Team,
2011),
RaoQ
and
CWM
were
computed
using
the
“FD”
package
(Laliberté
and
Shipley,
2011),
and
non-
parametric
post
hoc
used
the
“pgirmess”
package.
3.
Results
3.1.
Earthworm
density
and
species
richness
Eleven
species
were
found
in
the
four
agricultural
trials:
Lum-
bricus
castaneus
(Savigny,
1826),
Lumbricus
rubellus
(Hoffmeister,
1843),
Satchellius
mammalis
(Savigny,
1826),
Lumbricus
terrestris
(Linnaeus,
1758),
Aporrectodea
nocturna
(Evans,
1946),
Aporrec-
todea
longa
(Ude,
1885),
Aporrectodea
giardi
(Ribaucourt,
1901),
Allolobophora
chlorotica
(Savigny,
1826),
Aporrectodea
icterica
(Savigny,
1826),
Aporrectodea
caliginosa
(Savigny,
1826)
and
Apor-
rectodea
rosea
(Savigny,
1826).
In
three
of
four
trials,
total
earthworm
density
did
not
differ
significantly
between
tillage
types
for
a
given
trial
(Fig.
1).
Con-
versely,
in
trial
A,
1.77
times
more
individuals
were
retrieved
in
direct
seeding
plots
than
in
superficially
tilled
plots
and
1.97-fold
than
in
plowed
plots.
Three
species
displayed
density
differences.
In
trial
C,
A.
giardi
was
6
times
as
numerous
in
superficially
tilled
plots
as
in
tilled
plots.
In
trial
B,
18
times
as
many
individual
of
A.
chlorotica
were
collected
in
plowed
plots
as
in
direct
seeding
plots.
Regarding
L.
terrestris,
their
densities
were
found
to
be
promoted
in
ST
and
DS
plots
when
compared
to
P
plots
within
trials
A,
B
and
D.
The
ranges
of
increase
in
density
were
2–3×
and
6–15×
in
ST
and
DS
respectively.
High
values
of
L.
terrestris
densities
in
DS
plots
of
A
site
corresponded
to
juvenile
recruitment.
Within
the
four
sites,
the
mean
species
richness
was
not
influenced
by
tillage
type
(Table
5).
Conversely,
the
mean
species
richness
highly
varied
between
trials,
from
2.8
to
7.1
for
trials
C
and
A
respectively.
3.2.
Functional
diversity
3.2.1.
Eco-morphological
groups
density
L.
castaneus,
L.
rubellus
and
S.
mammalis
were
attributed
to
epigeic
earthworms,
L.
terrestris,
A.
nocturna,
A.
longa
and
A.
gia-
rdi
to
anecic
earthworms;
A.
chlorotica,
A.
icterica,
A.
caliginosa
and
A.
rosea
to
endogeic
earthworms
(Bouché,
1972).
No
statistical
dif-
ferences
were
observed
in
the
density
of
both
epigeic
and
endogeic
earthworms
between
tillage
types
within
a
trial
(Table
5).
Anecic
densities
increased
in
both
surface
tillage
and
direct
seeding.
When
compared
to
plowed
plots,
densities
were
1.8–3.2-fold
higher
in
surface
tilled
plots
and
4.4–5.4-fold
higher
in
direct
seeded
plots.
3.2.2.
Trait-based
indices
Values
of
RaoQ
ranged
from
0.04
to
0.1
on
all
the
experimental
trials
and
decreased
significantly
with
increasing
soil
tillage
inten-
sity
(Fig.
2).
Differences
between
RaoQ
of
the
two
most
extreme
management
types
were
significant
in
each
trial.
Superficial
tillage
showed
intermediate
values
between
the
two
extreme
types
of
soil
management.
Variability
of
RaoQ
was
low
in
direct
seeding
and
higher
in
plowed
plots
on
all
the
trials
(Fig.
3).
Three
morphological
traits
(i.e.
body
length,
epithelium
and
typhlosolis
types)
showed
similar
CWM
results
on
all
the
tri-
als
(Table
4).
An
increase
in
soil
tillage
intensity
increased
the
proportion
of
50–100
mm
long
earthworms
at
the
expense
of
smaller
(20–50
mm)
and
larger
(>100
mm)
earthworms,
and
favored
those
with
a
supple
epithelium
and
simple
typhlosolis.
Although
not
always
significant
(overlapping
confidence
inter-
vals),
results
tended
to
show
a
shift
from
smaller
(1–2
mm)
to
intermediate-sized
(2–4
mm)
cocoons
with
increased
tillage.
Effects
of
tillage
types
were
contradictory
between
trials
for
CWM
body
mass/length
ratio
for
the
class
1–7
and
7–15
mm
g−1.
Decrease
in
soil
tillage
intensity
increased
the
proportion
of
earthworms
with
a
body
mass/length
ratio
higher
than
15
mm
g−1.
Results
of
CWM
vertical
distribution
showed
that,
on
every
trial,
an
increase
in
tillage
intensity
led
to
a
decrease
in
the
proportion
of
earthworms
living
(i)
in
the
upper
soil
layer
(0–5
cm
depth)
and
(ii)
at
more
than
20
cm
depth.
Consequently,
it
favored
earthworms
living
between
5
and
20
cm
depth.
Concerning
carbon
preferences,
the
trends
of
the
two
first
classes
(<20
and
20–33.3
mg
kg−1)
were
contradictory
between
trials.
Significantly
fewer
earthworms
with
carbon
preferences
between
33.3
and
60
mg
kg−1were
found
in
the
plowed
plots
but
the
differences
were
small.
More
earthworms
with
carbon
preferences
higher
than
60
mg
kg−1were
retrieved

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx 5
Fig.
1.
Boxplots
of
species
number
for
the
different
types
of
soil
tillage:
direct
seeding
(DS);
superficial
tillage
(ST)
and
plowing
(P)
in
four
agricultural
trials
(A)–(D).
For
a
trial,
different
letters
indicate
statistical
differences
(p
<
0.05).
Fig.
2.
Boxplots
of
abundance
(individuals
m−2)
for
the
different
types
of
soil
tillage:
direct
seeding
(DS);
superficial
tillage
(ST)
and
plowing
(P)
in
four
agricultural
trials
(A)–(D).
For
a
trial,
different
letters
indicate
statistical
differences
(p
<
0.05).
Fig.
3.
Boxplots
of
RaoQ
entropy
for
the
different
types
of
soil
tillage:
direct
seeding
(DS);
superficial
tillage
(ST)
and
plowing
(P)
in
four
agricultural
trials
(A)–(D).
For
a
trial,
different
letters
indicate
statistical
differences
(p
<
0.05).

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
6C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx
Table
4
Confidence
interval
(mean
±
0.975
×
standard
deviation)
of
the
community
weighted
means
(CWM)
calculated
for
each
trait
attribute
on
each
agricultural
trial.
Confidence
intervals
followed
by
the
same
letter
overlap;
comparisons
are
made
between
all
tillage
types
within
a
trial
and
between
attributes
of
a
trait.
A
(Kerguehennec)
B
(Versailles)
C
(Mons)
D
(Thil)
Direct
seeding
Superficial
tillage
Plowing
Direct
seeding
Plowing
Superficial
tillage
Plowing
Direct
seeding
Superficial
tillage
Plowing
Body
length
(in
mm)
20–50
12.5–4.8
(ab)
13.7–15.5
(b)
10.8–13.5
(a)
11.6–15.5
(b)
0.1–10.0
(a)
13.7–15.9
(a)
9.5–14.2
(a)
10.5–17.0
(b)
7.6–11.3
(ab)
4.7–9.9
(a)
50–100 49.5–52.4 (a)
52.3–54.1 (a)
56–61.8 (b)
33.2–37.3 (a)
70.6–77.0 (b)
28.8–37.7 (a)
45.1–58.2
(b)
38.4–44.0
(a)
55.9–66.0
(b)
59.6–69.3
(b)
100–150
8.4–10.1
(b)
8.0–8.5
(b)
5.7–6.6
(a)
8.9–13.9
(b)
1.3–7.6
(a)
7.4–8.8
(a)
6.0–12.7
(a)
20.4–22.0
(b)
12.1–16.4
(a)
14.0–16.6
(a)
150–200
18.8–20.7
(a)
16.9–19.0
(a)
14.5–19.7
(a)
29.3–32.1
(b)
8.7–17.3
(a)
30.2–35.5
(b)
16.6–24.1
(a)
19.6–21.1
(b)
11.7–14.6
(a)
10.8–13.1
(a)
200–400 6.1–6.8 (a)
5.6–6.3
(a)
4.8–6.6
(a)
8.1–10.3
(b)
2.3–5.1
(a)
10.1–11.8
(b)
5.5–8.0
(a)
3.0–3.9
(c)
1.8–2.6
(b)
0.7–1.4
(a)
Body
mass/length
ratio
(in
g
mm−1)
1–7
33.2–35.2
(a)
36.9–39.7
(b)
34.6–39.2
(ab)
33.1–38.9
(a)
22.5–38.9
(a)
39.4–44.6
(a)
43.5–56.9
(a)
29.8–37.2
(a)
35.4–39.5
(a)
35.0–43.0
(a)
7–15
40.7–44.3
(ab)
37.3–41.6
(a)
44.2–47.8
(b)
33.2–40.1
(a)
53.6–66.7
(b)
32.2–35.3
(b)
17.8–25.7
(a)
23.2–31.4
(a)
34.1–38.2
(b)
33.3–40.9
(b)
>15
22.0–24.6
(b)
21.1–23.5
(b)
16–18.2
(a)
26.4–28.2
(b)
3.5–14.9
(a)
22.3–26.3
(a)
18.0–38.2
(a)
37.5–40.9
(b)
23.4–29.3
(a)
21.7–26.2
(a)
Cocoon
diameter
(in
mm)
1–2
7.5–10.3
(b)
7.9–9.4
(b)
5.9–7.3
(a)
7.7–10.3
(b)
0.1–6.7
(a)
0–0
(a)
0–0
(a)
6.9–10.8
(b)
5.1–7.6
(ab)
3.2–6.6
(a)
2–4
58.0–61.0
(a)
59.0–61.0
(a)
60.9–63.8
(a)
52.8–54.9
(a)
68.5–71.4
(b)
66.2–68.2
(a)
58–67.1
(a)
57.5–60.9
(a)
61.1–64.2
(b)
63.1–66.7
(b)
4–6
30.0–33.1
(a)
29.8–32.9
(a)
29.4–32.7
(a)
36.4–37.9
(b)
23.3–30.1
(a)
31.8–33.8
(a)
32.9–42.0
(a)
29.7–34.2
(a)
28.8–33.3
(a)
28.1–32.3
(a)
Epithelium
type
Supple
64.3–67.4
(a)
67.2–70.5
(ab)
67.8–75.3
(b)
46.3–51.3
(a)
71.5–86.2
(b)
44.1–52.2
(a)
55.4–71.6
(b)
49.1–52.2
(a)
62.9–71.3
(b)
64.5–70.1
(b)
Rigid
32.6–35.7 (b)
29.5–32.8
(ab)
24.7–32.2
(a)
48.7–53.7
(b)
13.8–28.5
(a)
47.8–55.9
(b)
28.4–44.6
(a)
47.8–50.9
(b)
28.7–37.1
(a)
29.9–35.5
(a)
Typhlosolis
type
Simple
45.9–50.7
(a)
50.6–52.8
(a)
55.2–61.6
(b)
28.5–33
(a)
69.6–74.6
(b)
44.1–52.2
(a)
55.4–71.6
(b)
29.6–36.4
(a)
48.2–60.8
(b)
51.7–63.5
(b)
Large
feather 49.3–54.1 (b)
47.2–49.4 (b)
38.4–44.8
(a)
67.0–71.5
(b)
25.4–30.4
(a)
47.8–55.9
(b)
28.4–44.6
(a)
63.6–70.4
(b)
39.2–51.8
(a)
36.5–48.3
(a)
Carbon
preferences
(in
mg
kg−1)
<20
4.6–4.8
(ab)
4.7–4.7
(a)
4.7–4.9
(b)
4.9–5.1
(a)
4.9–5.2
(a)
5.0–5.0
(b)
4.6–4.8
(a)
4.8–4.8
(a)
4.9–5.0
(b)
5.1–5.2
(c)
20–33.3 31.1–31.7 (a)
30.9–31.6 (a)
31.7–31.9 (b)
29.6–30.6
(a)
29.4–30.4
(a)
29.2–29.4
(a)
29.7–30.7
(b)
30.6–31.0
(b)
30.4–31.4
(ab)
30.3–30.6
(a)
33.3–60
48.7–48.7
(b)
48.4–48.5
(ab)
48.1–48.5
(a)
49.4–50.1
(b)
47.7–48.9
(a)
50.4–51.1
(b)
48.6–49.3
(a)
47.7–48.0
(c)
47.0–47.2
(b)
46.5–46.9
(a)
>60
14.9–15.6
(a)
15.2–16.0
(a)
14.8–15.4
(a)
14.6–15.5
(a)
15.6–17.9
(b)
14.7–15.3
(a)
15.5–16.8
(b)
16.2–16.9
(a)
16.7–17.5
(a)
17.5–18
(b)
Vertical
distribution
(in
m)
0–5
37.6–40.3
(b)
37.1–40.7
(b)
33.7–36.2
(a)
40.4–44.7
(a)
33.0–43.2
(a)
24.9–26.2
(a)
22.2–26.5
(a)
40.2–46.4
(b)
35.2–41.4
(ab)
31.9–38.7
(a)
5–20
46.5–48.7
(a)
47.1–49.4
(a)
51.2–52.5
(b)
38.9–42.4
(a)
48.2–54.4
(b)
51.2–54.0
(a)
56.1–60.8
(b)
37.5–42.7
(a)
44.4–51.6
(b)
46.4–53.0
(b)
>20
13.1–13.8 (a)
12.1–13.5 (a)
12.1–14.2
(a)
15.9–17.8
(b)
8.6–12.7
(a)
21.0–22.7
(b)
16.5–17.8
(a)
16.0–17.3
(b)
13.0–14.5
(a)
14.4–15.6
(a)

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx 7
Table
5
Density
(mean
and
standard
errors)
of
earthworm
species,
ecomorphological
groups
and
species
richness
in
plots
subjected
to
different
tillage
type,
over
4
agricultural
trials
(A,
B,
C
and
D).
Within
a
trial,
bold
values
with
letters
indicate
significant
differences
(p
<
0.05).
DS
for
direct
seeding,
ST
for
superficial
tillage
and
p
for
plowing.
Site
A
B
C
D
Tillage
type
DS
ST
P
DS
P
ST
P
DS
ST
P
Epigeics
L.
castaneus 15.8
(2.5) 10.9
(2.5) 6.1
(1.8)
15.6
(3.1)
7.5
(1.9)
0.0
(0.0)
0.0
(0.0)
7.9
(1.9)
2.6
(1.9)
1.6
(0.6)
L.
rubellus
2.6
(0.6)
0.9
(0.6)
0.3
(0.3)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
S.
mammalis 0.9
(0.4) 0.2
(0.4) 0.0
(0.1) 0.0
(0.0) 0.0
(0.0) 0.0
(0.0) 0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
Total
19.4
(3.0)
12.0
(3.0)
6.3
(1.9)
15.6
(3.1)
7.5
(1.9)
0.0
(0.0)
0.0
(0.0)
7.9
(1.9)
2.6
(1.9)
1.6
(0.6)
Anecics
A.
giardi 12.2
(1.8) 6.6
(1.8) 8.0
(1.4) 20.8
(3.3) 5.9
(1.8) 21.4
(0.0)a 3.5
(4.4)b 0.0
(0.0) 0.0
(0.0)
0.0
(0.0)
A.
longa
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
19.8
(6.7)
2.8
(0.9)
0.0
(0.0)
0.0
(0.0)
0.7
(0.5)
0.0
(0.5)
0.0
(0.0)
A.
nocturna
0.6
(0.4)
0.0
(0.4)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
0.0
(0.0)
24.5
(4.3)
10.9
(4.3)
6.6
(2.8)
L.
terrestris
88.4
(4.0)a
35.0
(4.0)ab
15.1
(2.0)b
34.4
(3.9)a
5.3
(1.1)b
13.8
(0.0)
7.5
(2.1)
9.4
(3.7)a
2.0
(3.7)ab
0.6
(0.5)b
Total
101.3
(5.1)a
41.6
(5.1)ab
23.1
(2.8)b
75.0
(9.1)a
14.1
(2.0)b
35.2
(0.0)a
10.9
(6.0)b
34.5
(6.3)a
12.9
(6.3)ab
7.3
(2.9)b
Endogeics
A.
chlorotica 6.5
(2.6) 10.2
(2.6) 7.1
(6.3) 1.3
(0.8) 24.4
(3.0)
0.0
(0.0)
0.0
(0.0)
1.4
(0.5)
1.7
(0.5)
1.6
(0.5)
A.
caliginosa
113.6
(12.5)
79.2
(12.5)
75.7
(9.9)
58.4
(10.3)
84.8
(7.8)
19.8
(0)
43.8
(4)
7.1
(1.9)
17.5
(1.9)
9.0
(4.4)
A.
icterica
33.1
(4.3)
12.6
(4.3)
20.7
(2.5)
4.1
(0.9)
6.4
(1.4)
0.0
(0.0)
0.0
(0.0)
1.7
(0.7)
1.2
(0.7)
0.8
(0.6)
A.
yyyrosea
3.4
(0.6)
2.5
(0.6)
1.9
(0.5)
0.0
(0.0)
0.0
(0.0)
22.3
(0.0)
12.8
(3.4)
0.1
(0.1)
0.0
(0.1)
0.0
(0.0)
Total
156.6
(17.1)
104.5
(17.1)
105.4
(14.6)
63.8
(10.3)
115.6
(9.5)
42.1
(0.0)
56.6
(4.9)
10.3
(2.5)
20.4
(2.5)
11.5
(4.5)
Species
richness
(species
per
m−2)
7.50
(0.43)
7.17
(0.40)
6.67
(0.42)
4.50
(0.29)
4.25
(0.48)
3.05
(0.17)
2.63
(0.28)
5.43
(0.57)
5.00
(0.38)
4.57
(0.72)
from
plowed
plots,
except
in
trial
A
where
no
significant
differences
were
found
between
the
three
tillage
types.
4.
Discussion
Whereas
many
studies
have
been
dedicated
to
plant
functional
trait
responses
to
disturbance,
relatively
little
was
known
on
the
causal
relationship
between
environmental
factors
and
functional
traits
of
soil
invertebrates,
e.g.
for
spiders
(Lambeets
et
al.,
2009),
ground
beetles
(Ribera
et
al.,
2001)
or
earthworms
(De
Lange
et
al.,
2013;
Fournier
et
al.,
2012).
Adding
to
this
emerging
body
of
evidence,
a
first
important
result
was
that
a
decrease
in
soil
tillage
intensity
led
to
an
increase
in
functional
diversity
and
to
changes
in
trait
profiles
of
earthworm
communities.
It
confirms
our
second
hypothesis
that
tillage
acts
as
an
environmental
filter.
Decreasing
the
intensity
of
tillage
caused
a
lesser
convergence
of
traits
and
thus
resulted
in
higher
functional
trait
diversity,
as
evi-
denced
by
the
Rao’s
Q
results.
Since
species’
functional
traits
can
be
regarded
as
links
between
diversity
and
ecosystem
function-
ing,
trait-based
indices
complement
structural
or
compositional
measures
of
diversity
by
providing
indirect
information
on
soil
eco-
logical
functioning.
Conceptually,
functional
traits
can
be
response
and/or
effect
traits
(Lavorel
and
Garnier,
2002).
We
did
not
assess
any
mechanistic
linkage
between
earthworm
response
traits
that
can
be
also
effect
traits
(e.g.
body
shape
and
vertical
distribu-
tion)
in
terms
of
soil
functioning.
Further
research
is
needed
to
test
the
hypothesis
that
communities
characterized
by
higher
functional
earthworm
diversity
enhance
agroecosystem
function-
ing.
A
second
important
result
was
that
soil
type
and
climate
had
only
a
small
effect
on
functional
trait
diversity
while
greatly
influ-
encing
earthworm
species
number,
density
and
ecomorphological
groups
as
shown
by
the
large
differences
within
and
between
tri-
als.
Our
first
hypothesis
was
only
partly
confirmed
since
amongst
ecomorphological
groups,
only
the
density
of
anecics
was
posi-
tively
influenced
by
the
decrease
in
soil
tillage.
The
usefulness
of
the
present
trait-based
approach
in
assessing
cultural
prac-
tice
effects
on
earthworm
communities
is
thus
reinforced
by
the
non-significant
differences
in
common
community
indices
like
abundance,
species
number,
and
the
abundance
of
individu-
als
of
two
ecomorphological
groups
(epigeic
and
endogeic).
That
anecic
abundance
is
positively
increased
by
decreasing
the
inten-
sity
of
tillage
has
already
been
demonstrated
(Capowiez
et
al.,
2009;
Simonsen
et
al.,
2011).
However,
in
the
present
case,
anecic
response
was
mainly
driven
by
the
effect
of
one
species,
A.giardi
in
trial
C,
L.
terrestris
in
the
other
sites.
Patterns
of
CWM
of
body
length,
vertical
distribution,
epithe-
lium
type
and
typhlosolis
type
were
consistent
between
trials
and
thus
across
the
studied
soil
and
climatic
contexts.
The
first
two
traits
were
used
by
Bouché
(1972)
to
define
earthworm
ecomor-
phological
class.
The
types
of
epithelium
and
typhlosolis
stand
out
from
the
rest
as
reliable
traits
for
understanding
the
responses
to
physical
disturbances.
Furthermore,
when
combined
with
ecomor-
phological
groups
(i.e.
epigeic,
anecic,
and
endogeic),
functional
trait
diversity
may
allow
us
to
identify
how
much
a
given
trait
is
affected
by
environmental
stress.
However,
we
lack
adequate
understanding
of
how
individual
traits
are
associated
and
how
this
lack
of
independence
among
traits
reflects
phylogenetic
(evo-
lutionary)
rather
than
ecological
constraints
(Poff
et
al.,
2006).
In
spite
of
this
limitation,
an
ecological
assessment
can
be
made
using
the
magnitude
of
changes
in
functional
traits
(e.g.
growth,
reproduction,
colonization
abilities
or
ecological
preferences;
see
e.g.
Baird
et
al.,
2008).
Such
a
procedure
has,
for
example,
been
used
to
determine
the
proportion
of
species
at
risk
(Pérès
et
al.,
2011).

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
8C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx
Minimum
tillage
promoted
the
maintenance
in
plots
of
both
small
and
large
earthworms
(<5
cm
and
>10
cm,
respectively),
with
a
high
body
mass/length
ratio,
able
to
live
either
in
the
top
5
cm
of
soil
or
below
20
cm.
In
addition,
these
earthworms
were
char-
acterized
by
a
rigid
epithelium.
It
confirms
our
hypotheses
(3.1)
that
the
largest
and
the
most
fragile
(with
a
supple
epithelium)
organisms
are
most
affected
by
intensive
tillage
and
(3.4)
that
the
more
an
individual
lives
in
the
topsoil,
the
more
it
suffers
from
plowing.
It
agrees
with
Chan
(2001)
who
suggested
that
“ploughing
reduced
the
number
of
the
large-bodied
anecid
species
by
mechanical
damage
and
destruction
of
the
burrows”
but
that
“the
small
bodied
species
were
able
to
survive
better
in
the
ploughed
soil
than
the
anecid
species”.
Indeed,
intermediate-size
earthworms
living
preferentially
between
5
and
20
cm
depth
seemed
to
be
favored
by
plowing,
i.e.
A.
icterica,
A.
caliginosa
and
A.
rosea.
These
earthworms
may
benefit
from
crop
residue
incorporation
(Chan,
2001;
Pelosi
et
al.,
2009).
The
greater
abundance
of
earthworms
with
a
supple
epithelium
in
the
plowed
plots
might
be
explained
by
a
higher
resistance
to
physical
disturbance
(soil
inversion
or
plow
share
damage)
perhaps
because
they
are
less
sensitive
to
mechanical
constraints
through
elasticity.
Besides,
earthworms
with
a
rigid
epithelium
would
be
more
adapted
to
the
unplowed
soils,
where
soil
bulk
density
is
generally
higher
(Soane
et
al.,
2012).
The
higher
proportion
of
earthworms
with
a
ramified
typhlolo-
sis
was
recorded
in
unplowed
plots
whereas
we
hypothesized
(3.2)
that
more
earthworms
with
a
larger
feather
typhlosolis
would
be
found
in
plowed
plots,
since
it
would
favor
a
higher
assimilation
of
nutrients
(Stevens
and
Hume,
1995).
This
result
could
be
linked
to
the
quality,
quantity
or
localization
of
organic
matter
in
the
soil.
Tebrüge
and
Düring
(1999)
showed
for
instance
that
the
total
carbon
content
and
the
degree
of
incorporation
of
crop
residues,
respectively,
were
the
same
under
plowing
and
superficial
tillage
or
direct
seeding
but
the
distribution
within
the
soil
profile
was
different.
We
can
also
propose
that
soil
organic
matter
is
more
labile
in
plowed
soils,
selecting
more
individuals
requiring
a
lesser
investment
in
digestion
process.
The
hypothesis
(3.3)
that
a
higher
proportion
of
earthworms
with
high
soil
carbon
content
requirement
would
be
collected
in
unplowed
plots
was
confirmed
in
all
sites
for
the
class
of
Corg
content
between
33
and
60
mg
g−1.
However,
contradictory
results
were
obtained
for
the
other
classes,
for
instance
the
class
>60
mg
g−1.
An
important
drawback
is
the
arbitrariness
of
the
num-
ber
of
classes
and
of
the
boundaries
of
such
classes.
More
generally,
it
poses
the
challenge
of
creating
a
shared
thesaurus
of
traits
and
their
classes.
Acknowledgements
We
would
like
to
thank
all
the
people
who
took
part
in
the
earthworm
sampling
and
especially
the
technical
team
of
the
INRA
UMR
PESSAC
of
Versailles
(Jean-Pierre
Pétraud,
Christelle
Mar-
rauld,
Virginie
Grondin
and
Jodie
Thénard),
Hubert
Boizard
and
the
technical
team
of
Estées-Mons,
the
Brittany
Chambers
of
Agricul-
ture,
in
particular
Dr.
Djilali
Heddadj
and
Patrice
Cotinet,
and
the
technical
team
of
ISARA
Lyon.
The
authors
wish
to
thank
the
Fonda-
tion
pour
la
Recherche
sur
la
Biodiversité
(FRB)
for
their
financial
support
and
the
colleagues
of
BETSI
project
for
valuable
discus-
sions.
We
would
also
like
to
thank
Alan
Scaife
for
revising
the
English.
Appendix
1.
List
of
functional
traits
for
the
different
earthworm
species
Species
Body
Length
(cm)
Body
mass/length
ratio
(in
g
mm−1)
Cocoon
diameter
(in
mm)
Epithelium
type
Typhlosolis
type
Carbon
preferences
(in
mg
kg−1)
Vertical
distribution
(in
cm)
20–50
50–100
100–150
150–200
200–400
1–7
7–15
>15
1–2
2–4
4–6
Supple
Rigid
Simple
Large
feather
<20
20–33.3
33.3–60
>60
0–5
5–20
>20
Allobophora
chlorotica
0
100
0
0
0
0
100
0
0
100
0
100
0
100
0
5
26
49
21
60
40
0
Aporrectodea
caliginosa
0
100
0
0
0
67
33
0
0
60
40
100
0
100
0
5
30
46
19
20
70
10
Aporrectodea
giardi 0
0
0
75
25
0
100
0
0
67
33
0
100
0
100
7
26
55
12
33
33
33
Aporrectodea
icterica
0
100
0
0
0
0
100
0
0
73
27
100
0
100
0
4
43
47
6
10
80
10
Aporrectodea
longa
0
0
50
50
0
0
60
40
0
67
33
0
100
0
100
4
28
57
11
33
33
33
Aporrectodea
nocturna
0
17
50
33
0
0
33
67
0
73
27
0
100
0
100
6
30
47
17
33
33
33
Aporrectodea
rosea
50
50
0
0
0
100
0
0
0
100
0
100
0
100
0
4
28
49
19
10
70
20
Lumbricus
castaneus
75
25
0
0
0
100
0
0
50
50
0
100
0
0
100
4
28
46
22
100
0
0
Lumbricus
rubellus
0
60
40
0
0
0
75
25
50
50
0
100
0
0
100
2
19
46
33
80
20
0
Lumbricus
terrestris
0
0
33
50
17
0
0
100
0
33
67
0
100
0
100
4
33
52
11
40
40
20
Satchellius
mammalis
100
0
0
0
0
100
0
0
60
40
0
100
0
0
100
4
24
57
15
100
0
0

Please
cite
this
article
in
press
as:
Pelosi,
C.,
et
al.,
Reducing
tillage
in
cultivated
fields
increases
earthworm
functional
diversity.
Appl.
Soil
Ecol.
(2013),
http://dx.doi.org/10.1016/j.apsoil.2013.10.005
ARTICLE IN PRESS
G
Model
APSOIL-1935;
No.
of
Pages
9
C.
Pelosi
et
al.
/
Applied
Soil
Ecology
xxx (2013) xxx–
xxx 9
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