Soil Biology & Biochemistry 55 (2012) 93e103

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Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Role of earthworms in regenerating soil structure after compaction in reduced

tillage systems
Capowiez Yvan a, *, Samartino Stéphane b, Cadoux Stéphane c, Bouchant Pierre c, Richard Guy d,
Boizard Hubert c
a
INRA, UR 1115 Plantes et Systèmes Horticoles, Domaine Saint Paul, 84914 Avignon Cedex 09, France
b
INRA, UMR Climat-Sol-Environnement, Domaine Saint Paul, 84914 Avignon Cedex 09, France
c
INRA, US 1158 Agro-Impact, 2 Chaussée Brunehaut, Estrées-Mons, BP 50136, 80203 Péronne Cedex, France
d
INRA, UR 0272 Science du Sol, 45166 Olivet, France

a r t i c l e i n f o a b s t r a c t

Article history: New non-tillage or reduced tillage agricultural practises are being increasingly adopted but generally
Received 30 March 2012 result in higher soil compaction. Due to their recognised physical influence mainly through burrow
Received in revised form creation, it is often claimed that earthworm activity could alleviate soil compaction in these systems. To
13 June 2012
put this assumption to the test, an experimental compaction event was carried out on one plot of arable
Accepted 18 June 2012
land. The abundance and biomass of earthworms were evaluated in compacted (under wheel tracks) and
Available online 7 July 2012
non-compacted (between wheel tracks) zones, seven times over a two-year period. In addition, the
functional consequences of earthworm activity, defined by burrow abundance assessed in 2D and 3D and
Keywords:
X-ray tomography
water infiltration, were measured three times over the same period. The short-term (less than three
Water infiltration months) effects of the compaction were clear: soil bulk density increased from 1.46 to 1.57 g cm
3, the
Earthworm burrow abundance and biomass of earthworms were greatly reduced (
40% and
70% respectively) and the
Recovery number and continuity of macroporosity were lower under wheel tracks at least until a depth of 30 cm.
After these initial detrimental effects, we observed a rapid recovery of earthworm populations with no
statistical difference between compacted and control zones more than three months after the
compaction. However, the recovery of soil functional properties linked to earthworm activity, macro-
porosity and water infiltration, was much slower and took between 12 and 24 months. Despite these
modifications, there were no significant changes in soil bulk density with time during the two-year
period. This study demonstrates that earthworms are important actors in the regeneration of com-
pacted soil. Although the complete regeneration of compacted soil by earthworms is a slow process,
agricultural practises that promote earthworm density and activity should be encouraged in reduced or
minimum tillage systems.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction
Compaction is an important threat to arable land (Soane and van
Ouwerkerk, 1994). Compaction is mainly due to the use of heavy
machinery which leads to severe changes to the soil structure and
thus modifies its functioning (Horn et al., 2000). As the use of tillage
can be expensive in terms of power requirements and fuel usage,
time and capital costs (McHugh et al., 2009), alternative agricul-
tural practices such as minimum or reduced tillage are being
increasingly adopted. These new tillage systems also have positive
environmental impacts: organic matter is concentrated at the soil
* Corresponding author.
E-mail address: yvan.capowiez@avignon.inra.fr (C. Yvan).
surface and soil erosion is reduced (Cannell and Hawes, 1994). In
oceanic climates, however, compaction is also frequently due to
wet conditions in spring and autumn when crops such as maize or
sugar beet are sown and harvested (Boizard et al., 2002). Under
minimum or reduced tillage, these compacted zones are expected
to regenerate naturally under the influence of climatic (alternating
dry/wet and freeze/thaw cycles) and soil biological actors (mainly
roots and earthworms) (Drewry, 2006).
The main influence of earthworms in soil is the modification of
soil structure through the creation of burrows (Capowiez et al.,
2003) and the production of casts (Blanchart et al., 2004; Jouquet
et al., 2008). It is thus generally claimed that earthworms can
contribute to the regeneration of compacted zones by burrowing
through these zones and this was demonstrated under laboratory
conditions (Joschko et al., 1989; Zund et al., 1997; Langmaack et al.,

0038-0717/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.soilbio.2012.06.013
94 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103
1999; Jégou et al., 2002) and under semi-field conditions (Capowiez
et al., 2009a). Nevertheless evidence for their direct role in regen-
erating compacted soils under natural conditions is still lacking and
the first experiments carried out under tropical (Blanchart et al.,
1994), forest (Muys et al., 1992) or crop (Radford et al., 2007)
conditions failed to show a significant effect of earthworms.
Aside from the inherent variability of studies under natural
conditions and the difficulty in distinguishing naturally entangled
factors, the important difference between laboratory and field
studies is that earthworms can not avoid the compacted soils under
laboratory conditions. Indeed, Stovold et al. (2004) and Capowiez
et al. (2009a) showed that earthworms preferentially avoid these
zones in controlled or semi-field conditions. Thus most of the
laboratory studies demonstrated that earthworms are able to
burrow in very compacted zones but did not show their actual
capacity to regenerate these zones under natural conditions. In
addition, it is now well established that compaction, and thus soil
bulk density, is an important factor limiting earthworm abundance
in arable soils (Chan and Barchia, 2007; Ouellet et al., 2008; Beylich
et al., 2010). Radford et al. (2001) estimated the natural regenera-
tion of compacted soils and concluded that earthworms play
a limited role since earthworm density remained low in compacted
plots. However, in their experiment, plots were homogeneously
compacted and this may have slowed down or prevented earth-
worm recolonisation. Under real management conditions,
compaction is spatially heterogeneous either horizontally (wheel
tracks) or vertically (plough pan) (Roger-Estrade et al., 2009).
To determine the actual role of earthworms in regenerating
compacted zones, it is thus crucial to carry out a study under
natural conditions with realistic soil bulk densities, possibilities for
avoidance of these zones and natural climatic variations which can
influence both earthworm behaviour and the fate of compacted
zones. The regeneration of compacted zones, or the resilience of the
soil, is a dynamic process and may be different depending on the
factor under consideration (Gregory et al., 2009). To accurately
describe the role of earthworms, it is therefore crucial (i) not to
focus on only one factor (for example earthworm abundance) but
also the functional consequences of their activity and (ii) to study
regeneration rates and establish the time necessary to return to
equilibrium, i.e. the engineering resilience according to Holling
(1996).
To this aim, we carried out a field study by creating a pattern of
compacted and non-compacted lanes in one arable plot. We then
studied (i) the short-term changes (the first 3 months) in term of
soil bulk density and earthworm biomass and abundance and (ii)
the long-term (from 3 months to 2 years) recovery of the earth-
worm community and the compacted soil by following earthworm
biomass and abundance but also earthworm-related macroporosity
(either in 2D and in 3D) and water infiltration using the Beer-Kan
method.
2. Materials and methods
2.1. Site description
The experiment was carried out at the long-term experimental
site: “cropping systems and soil structure” located in northern
France (Estrées-Mons, 50 N latitude, 3 E longitude, 85 m a.s.l.)
(Boizard et al., 2002). The 0e30 cm horizon has a silt loam texture
(19% clay, 76% silt, 5% sand and 1.7% organic carbon) and a pH of 7.6.
The gravimetric soil water contents measured
at
10,
32,
50,
100 and
1500 kPa were 0.253, 0.229, 0.208,
0.175 and 0.084 g g
1 respectively. Water content at field capacity,
measured in the field 2e3 days after excess water had drained away
during the winter season (Hillel, 1971), was 0.24 g g
1. The average
air temperature is 10.3  C and the annual rainfall is 667 mm.
The experiment was conducted as part of the long-term
“Cropping systems and Soil Structure” field experiment (Boizard
et al., 2002). Three cropping systems were compared between
1999 and 2008 with a wide range of soil compaction intensities,
depending on crop rotation and the rules of decision making. In
1999, a new treatment with superficial tillage at a depth of less than
10 cm was introduced in the experiment in order to compare the
effects of annual ploughing and reduced tillage on soil structure
evolution.
In 2005 we selected one 0.7 ha plot with reduced tillage to carry
out the study. Rotation from 2005 to 2008 was pea (Pisum sativum
L.)/winter wheat (Triticum aestivum)/flax (Linum Usitatissimum)/
winter wheat. The risk of compaction was low in this rotation
because harvesting was always carried out in summer, i.e. during
a dry period of the year, and sowing by avoiding wet conditions in
spring. Seedbed preparation was performed with a short disc
harrow and sowing with a combined rotary harrow and disc drill.
The mean depth of stubble tillage and seedbed preparation was
6 cm and varied between 4 and 8 cm. We evaluate compaction
using a morphological description of the tilled layer (Boizard et al.,
2002). The proportion of highly compacted zones, as the ratio of the
area of the structure considered to the total area of the tilled layer
under the seedbed, was only 20% in 2005. The cultural operations
during the three following years were made in rather dry condi-
tions and the proportion of highly compacted zones remained low.
2.2. The compaction event
A controlled compaction was carried out on the 8th of February
2005. We created a pattern of compacted and non-compacted lanes
by wheeling a tractor, equipped with a combined power harrow
and a drill in transport position, in wet conditions. Two 25 m long
passages were made side by side with the tractor under wet soil
conditions. The total load was approximately eight tonnes and the
rear wheel pressure was 250 kPa. The mean stress at the soil surface
under the wheel tracks was 120 kPa. The soil water content at the
time of the compaction was on average 26.2% and 23.1% between
0e5 and 5e30 cm, respectively. These values are close to the soil
water content at field capacity, which is 24% in this silt loam soil. In
order to ensure the creation of a massive compacted structure,
a second compaction passage was carried out a week later, using
the same device and the same tools. The soil water content at the
time of the second compaction was on average 26.3% and 23.4%
between 0e5 and 5e30 cm, respectively, outside the wheel tracks
and 29.0% and 25.5% between 0e5 and 5e30 cm, respectively,
under the wheel tracks. Given the width of the wheels (0.55 m) and
the path of the tractor (1.95 m), 36% of the area was affected by
wheel tracks and thus severely compacted. In representative tillage
systems in northern France, the surface affected by wheel tracks
with similar constraints is between 20 and 30% at harvesting for
winter wheat and between 62 and 68% at harvesting for sugar beet
(Godin, 2005). The locations of the compacted zones were recorded
with precision in order to locate them at each subsequent
measurement. The different measurements used to quantify the
regeneration dynamics were made advancing steadily along the
25 m of compaction, with at least 2 m between each data point.
2.3. Soil porosity
The soil bulk density was determined on 6 undisturbed cores
(0.05 m diameter, 0.05 m long) at three depths (0.10, 0.15 and
0.20 m) after each sowing outside and under the wheel tracks at
two dates (March 2005 and March 2007, i.e. respectively two and 24
 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103
months after the compaction event). Total porosity estimated from
the bulk density was divided into the textural and structural pore
space. The structural porosity (nS) was calculated from dry bulk
density measurements in the field using the following formula:
nS ¼ 1
ra =rt ðWÞ (1)

3
with ra the soil bulk density (g cm ) and rt(w) the textural soil
density (g cm
3) at a water content w at the time of bulk density
measurement. The textural soil density was measured as a function
of soil water content using 2e3 mm aggregates to consider only the
pore space due the particle arrangements and not tillage or
weathering (Monnier et al., 1973). The initially saturated aggregates
were gradually dried to zero water content, and 2e3 g samples
were regularly taken for the determination of volume and dry mass.
The textural soil density at a given water content was then obtained
from the ratio of the dry mass of the sample to its volume at that
water content.
2.4. Initial effect of the compaction on macropore number and
continuity
In March of 2005, two months after compaction, the short-term
effects of the compaction on the bulk density and continuity of
macropores and the maximal depth of these effects (Table 1) were
determined. Four PVC rings (diameter ¼ 0.4 m) were inserted into
the soil (two in compacted and two in control zones). We con-
ducted an infiltration experiment using the single-ring infiltration
method (see below) to assess macropore continuity, using methy-
lene blue added to the water (concentration ¼ 0.01 M) as a dye
tracer of conductive macropores (Hangen et al., 2002; Chan, 2004).
At the end of the infiltration experiment, the soil below the PVC
rings was excavated with a spade in order to prepare successive
horizontal planes at 10, 20, 30 and 45 cm depth. The 30 cm depth
plane was adjusted to correspond to the depth of the old plough
pan. For each depth, the plane was carefully refreshed with a knife
and the soil was removed using a vacuum cleaner. Macropores
stained in blue were marked with a coloured pin. The soil surface
was then photographed. On the images, each visible round-shaped
macropore was traced manually using the freeware NIH-Image
(Rasband and Bright, 1995) and labelled as stained or not (accord-
ing to the presence of pins). Given the diameter of the PVC ring, the
area of each macropore was automatically computed and pores,
whose Equivalent Circular Diameter (ECD) was smaller than 2 mm,
were discarded since such pores are unlikely to be made by
earthworms.
Table 1
Summary of the measurements carried out in compacted and uncompacted zones (under and between wheel tracks) and their date (and number of months after compaction
between brackets). The compactions were done the 8th and 15th of February 2005.
Dates (and months after compaction) Measurements
March of 2005 (M þ 2) - Soil bulk density
(and March of 2006 (M þ 13))
- Infiltration (Beer-Kan) using methylene blue
- Macroporosity (2D) at 4 depths
21st of February 2005 (M þ 0) - Earthworm sampling
March of 2005 (M þ 1)
April of 2005 (M þ 2)
May of 2005 (M þ 3)
May of 2005 (M þ 3) - Macroporosity (2D) at one depth (
10 cm)
November of 2005 (M þ 9) - Earthworm sampling
March of 2006 (M þ 13)
March of 2007 (M þ 24)
May of 2005 (M þ 3) - Soil cores sampling þ X-ray tomography
November of 2005 (M þ 9) - Water infiltration (single-ring method)
March of 2007 (M þ 24)
95
2.5. Earthworm sampling and recolonisation dynamics
Earthworm communities were sampled to study the short-term
and the long-term effects of compaction (Table 1). For the short-
term study, earthworm communities were sampled a week, one,
two and three months after soil compaction. To examine long-term
effects, these communities were sampled 9, 13 and 24 months after
compaction excluding summer periods (i.e. when earthworms
were inactive). For each date, eight PVC rings (diameter ¼ 0.4 m)
were inserted in the soil, four in the compacted (under wheel
tracks) and four in the control zones. Approximately 5 l of diluted
mustard (15 g l
1) was poured into each PVC ring. The mustard
used contained 12% vinegar and approximately 0.4% allylisothio-
cyanate. All earthworms which came to the surface were sampled.
After 30 min, the soil was dug out to a depth of 0.3 m and hand-
sorted. Hand-sorting was carried out to ensure the representa-
tiveness of the earthworm sample (especially for endogeic species)
but as a consequence it was not possible to carry out other
measurements (macroporosity and water infiltration) in exactly the
same location. In the Estrées-Mons site, only four earthworm
species (two anecic Lumbricus terrestris, and Aporrectodea giardi,
and two endogeic Aporrectodea caliginosa and Aporrectodea rosea)
were very common and could be easily distinguished with the
naked eye after a first determination period using the key of Bouché
(1972). Very rarely Allolobophora chlorotica and Octolasion sp.
individuals were found. Very small endogeic earthworms (less than
0.1 g) that could not be clearly identified as either A. rosea or
A. caliginosa species were classified as ‘unidentified juvenile
endogeics’ (UJE). Overall, the earthworm community was highly
dominated by A. caliginosa (72.6%). The three other species were
less current with 10.4, 2.5 and 14.5% for A. rosea, A. giardi and
L. terrestris respectively.
2.6. Macroporosity dynamics
Three, 9, 13 and 24 months after compaction, the earthworm-
related macroporosity was estimated with the same method
described above (Section 2.4). This type of data is generally highly
variable and we chose to increase the number of replicates and
decrease the number of depths investigated. Thus we prepared
a 30 cm wide, 4 m length horizontal plane at 10 cm depth using
a spade. Orthogonally, this plane encompassed the two passages of
the wheel tracks and we were able to define different zones, the
compacted zones (under wheel tracks) and the non-compacted
zones (between wheel tracks). In each zone, we defined eight
different 20*20 cm areas using yellow marks. These areas were
Aims
Short-term effects of compaction on biological (
earthworm density) and physical characteristics
(macropore density and continuity, water infiltration)
Dynamics of the recovery regarding earthworm
density, macropores density (2D and 3D) and water infiltration
96 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103
then carefully refreshed with a knife and the soil was removed
using a vacuum cleaner. The surface was then photographed. The
pictures were analysed and each visible round-shaped macropore
was traced manually using NIH-Image (Rasband and Bright, 1995).
Given the diameter of the PVC ring, the area of each macropore was
automatically computed. Pores whose Equivalent Circular Diameter
(ECD) was smaller than 2 mm were discarded and the number of
pores were automatically counted for two size classes (between 2
and 4 mm ECD and above 4 mm ECD).
2.7. 3D investigation of the recolonisation of compacted zones by
macropores
One, 9 and 24 months after compaction, four soil cores (about
40 cm in length and 16 cm in diameter) were manually excavated,
two in the compacted zone (under wheel tracks) and two in the
control zone, following the procedure described by Bastardie et al.
(2005): (i) first, a large pit (0.5 m  0.5 m and 40 cm deep) was dug
in the field using a pick, keeping the central part of the pit area
undisturbed; (ii) next, the cylinder was carefully placed and pushed
around each undisturbed part of the soil by manual removal of
small increments of about 1 cm of soil using a knife. To avoid the
creation of new burrows after sampling, chloroform (30 ml) was
applied on each soil core to kill the earthworms. Soil cores were
then stored at 2  C to prevent emergence from cocoons before
analysis.
Each soil core was imaged using X-ray computed tomography
with a medical scanner (LightSpeed VCT, General Electrics) at the
Amiens hospital to obtain a set of 1.25 mm thick images every
1.25 mm. The X-ray beam was operated at 50 mA and 100 kV. The
burrow system in each core was reconstructed following the
method proposed by Pierret et al. (2002). In brief, macropores were
traced starting from the darkest voxels by studying local variation
in mean grey levels when the current voxel was included in the
current macropore. Macropores that were too small (less than 300
voxels, i.e. about 0.5 cm3) were discarded. At this stage, the volume
of macropores, and the number of burrows (a burrow is a set of
connected voxels) were computed.
For the sake of 3D rendering, we defined a point of observation
and computed the distance between this point and each voxel of
the macropores. By projecting these values on a vertical 2D image,
keeping the minimum values (meaning that the nearest macro-
pores hide all the macropores behind them) then subsequently
translating distance into a gradient colour map (here yellow for the
minimum and blue for the maximum), we can visualise the
resulting earthworm burrow systems in 3D. When the superficial
tillage was recent, the first images coming from X-ray tomography
were removed since this layer was very fragile and made of loose
soil with a high global porosity in which it is difficult to assess with
certainty which macropores were made by earthworms.
2.8. Water infiltration measurements
One, 9 and 24 months after compaction, the effects of earth-
worm activity on soil macroporosity and water infiltration were
determined. Firstly, 2e3 cm of the soil was removed using a spade
and a flat horizontal plane was prepared and refreshed using
a knife. Water infiltration was examined in each plot using the
single-ring infiltration method (Braud et al., 2005), which was
preferred to double-ring methods since it was less time-consuming
and easier to do. This method was applied in this study to quite
a large area (0.125 m2) to take into account the heterogeneity of the
spatial distribution of earthworm macropores. At each date, eight
PVC rings (diameter ¼ 0.4 m), four in the compacted zone and four
in the control zone, were inserted in the soil to a depth of about
1e2 cm. A fixed volume of water was poured into the ring at time
zero and the time elapsed for the known volume of water to infil-
trate was measured. When the first volume had infiltrated
completely, a second fixed volume of water was added. The pres-
sure head imposed at the soil surface was considered as constant,
ranging from 10 mm to 0 mm. The procedure was repeated for
a series of about eight to ten known volumes until an apparent
steady state of infiltration (i.e. the time elapsed between two
volume additions was constant) was reached. We computed the
final infiltration rate FIR (mm h
1) by estimating the slope (linear
regression) of the relationships between cumulative infiltration
and time elapsed at steady state. As the FIR was analysed on
a relative basis (compacted vs control zones), we assumed that
conclusions made concerning the FIR could be extended to soil
permeability (Capowiez et al., 2009b).
2.9. Statistical analysis
Homoscedasticity and normality were verified using Bartlett
and ShapiroeWilk tests. In most cases, data were log-transformed
due to variance heterogeneity. Soil bulk density were analysed
independently for each depth with a two-way ANOVA with
compaction and date as factors. Structural porosities were
compared using a two-factor KruskaleWallis test. The initial effect
of compaction on the number of macropores was analysed with
a one-way ANOVA at each of the four depths. No statistical analysis
was applied to the rate of coloured macropores. Earthworm
abundance and biomass were analysed with 3 repeated measure-
ments ANOVA, with compaction as a factor, for three time periods
(0e2 months, 2e9 months and 13e24 months after compaction)
visually defined by the difference in mean values between com-
pacted and non-compacted zones. The number of macropores
during the recovery was analysed with a one-way ANOVA at each
date on the two pore size classes independently. No statistical
analysis was performed on the main characteristics of the burrow
systems obtained after 3D reconstruction due to the low number of
replicates. Data on water infiltration (FIR) was analysed using
a ManneWhitney test for each date.
3. Results
3.1. Initial effects of compaction on soil bulk density, macropore
number and continuity
The soil bulk density under wheel tracks, measured one month
after compaction, was significantly higher than under control zones
at 1.45 and 1.57 g cm
3 respectively (Table 2; F ¼ 50.31; df ¼ 1;
p < 0.0001). To better evaluate compaction intensity, we calculated
the structural pore space from the bulk density. Structural space
results from the arrangement of structural elements created by
tillage and weathering whereas the textural pore space is due to the
packing of elementary particles (Fiès and Stengel, 1981). The
structural porosity was less than 5% under wheel tracks meaning
that compaction was severe under wheel tracks. It was between 7
and 11.8% outside the wheel tracks. This was still the overall pattern
two years after the compaction event: the structural porosity
remained less than 5% at 10e15 cm and 20e25 cm depth, but
increased at 5e10 cm (Table 2).
The mean number of macropores in the control zones was
similar at 10 and 20 cm depth with an average of 350 m
2, but
decreased at 30 cm depth (183 m
2) and showed intermediate
values at 45 cm depth (290 m
2). The compaction significantly
decreased the number of macropores until a depth of 30 cm (Fig. 1;
F ¼ 8.21; df ¼ 1; p ¼ 0.09). The mean decrease was approximately
70, 65 and 27% at 10, 20 and 30 cm depth respectively. For each
 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103 97

Table 2
Mean soil bulk densities and soil structural porosities (þstandard deviation) in the compacted (under wheel tracks) and noncompacted (control) zones (n ¼ 6). Values bearing
different letters are significantly different at the 5% level (capital letters are used for global comparisons between compacted and control zones at each date and non capital
letters are used for comparisons between compacted and control zones at each depth and date; no significant interaction was found between date and depth at each date).

Date Depth (cm) Soil bulk density (g cm
3) Structural porosity (m3 m
3)

Compacted zone Control zone Compacted zone Control zone

March 2005 (one month after compaction) 5e10 1.58b (þ0.036) 1.50a (þ0.032) 2.22a (þ1.57) 5.44b (þ4.45)
10e15 1.58b (þ0.034) 1.46a (þ0.023) 2.64a (þ4.75) 9.31b (þ1.92)
20e25 1.55b (þ0.067) 1.42a (þ0.020) 4.11a (þ3.66) 11.54b (þ4.61)
Mean 1.57B 1.46A 2.99A 8.76B
March 2007 (24 months after compaction) 5e10 1.47a (þ0.064) 1.44a (þ0.089) 8.52a (þ4.58) 10.42b (þ3.95)
10e15 1.53b (þ0.064) 1.47a (þ0.040) 4.63a (þ2.49) 8.39b (þ4.02)
20e25 1.57a (þ0.061) 1.52a (þ0.045) 2.18a (þ2.78) 5.65b (þ3.82)
Mean 1.53B 1.48A 5.11A 8.15B

depth, the proportion of coloured macropores was generally lower
in the compacted zones compared to the control zones indicating
a decrease in macropore continuity to the surface.
3.2. Dynamics of earthworm abundance after soil compaction
Non-adult earthworm abundance was highly variable so only
adult abundance is presented here (Fig. 2A). Three time periods
were chosen for the statistical analysis: (i) the three first dates (one
week, one and two months after compaction) on which mean
abundance was higher in control zones, (ii) the two following dates
(3 and 9 months after compaction) on which abundance was much
higher, especially in compacted zones and (iii) the two last dates
(13 and 24 months after compaction). The three repeated
measurements ANOVAs revealed significant differences only for
the first phase where earthworm abundance was significantly
higher in control zones (F ¼ 7.84; df ¼ 1; p ¼ 0.031 for the main
factor).
For earthworm biomass (including non-adult earthworms), the
three phases were almost the same except for the very last date
(Fig. 2B). The three ANOVAs again revealed significant differences
only for the first temporal phase (one week, one and 2 months after
compaction) with a significantly higher biomass in control zones
(F ¼ 8.09; df ¼ 1; p ¼ 0.029 for the main factor). Due to the low
number of replicates at each date and to the high variability in the
data, we did not observe significant difference in the abundance or
biomass between species or ecological type (anecic and endogeic)
between control and compacted plots.
3.3. Evolution of the macroporosity (assessed in 2D)
During the two year period, the mean number of macropores at
10 cm depth ranged from 180 to 280 and from 44 to 94 m
2 for the
smaller (2e4 mm) and larger (>4 mm) class of pores, respectively
(Fig. 3). The mean number of macropores in the compacted zones
increased with time from 53 to 228 and from 15 to 75 m
2 for the
smaller and larger class of pores, respectively. In the control zone,
the number of macropores was fairly constant for both classes of
pores. The ANOVA carried out on each date showed a significantly
higher number of pores in the control zones from one week to 13
months after compaction and no significant difference for the last
date (24 months after compaction), for both classes of pores.
3.4. Dynamics of macropore recolonisation of compacted zones
(assessed in 3D)
The 3D reconstructions of the earthworms burrow systems
clearly illustrated (i) the initial destruction of macropores due to
compaction (Fig. 4; first row) and (ii) a progressive recolonisation
by macropores (Fig. 4 second and third rows). In all the recon-
structions, burrow systems consisted of a mixture of cylindrical
burrows with various diameters (likely to result from the activity of
juvenile endogeics to adults anecics) and less tubular macro-
porosity likely to result from older, more or less destroyed, mac-
ropores. This less tubular porosity is also particularly visible in the
two soil cores from the compacted zones excavated one month
after the compaction.

Fig. 1. Short-term effect of compaction on macropore number (assessed on 2D planes at different depths) and continuity (estimated by the proportion of coloured macropores) in
March 2005 (2 months after compaction).
98 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103

Fig. 2. Abundance of adult earthworms (A) and total earthworm biomass (B) at each sampling date under wheel tracks (compacted) and between wheel tracks (control). A star
indicates a significant difference between compacted and control (three time periods were considered: 0e2, 3e9 and 14e23 months after compaction).

These visual differences were then quantified as shown in Fig. 5.
Statistical analysis was not possible due to the low number of cores
excavated at each date, however clear trends were still observed.
The macroporosity increased gradually with time (Fig. 5A) from 31
to 198 cm3 in the compacted zone and ranged from 118 to 173 cm3
in the control zone (mean value for soil core whose surface area is
about 0.018 m2). The number of burrows with a vertical extension
larger than 5 cm evolved with time in the compacted zone: initially
very low (4.6-fold less than in control zone), they increased eight
months after the compaction (1.7-fold less than in control zone)
and became higher than in the control zone 24 months after the
compaction. The number of macropores with a volume greater than
0.5 cm3 showed the same trend as the total macroporosity volume
with a progressive increase with time (Fig. 5C).
3.5. Impact on the rate of water infiltration
The final water infiltration rates followed a clear pattern with
time: one and eight months after compaction, the rate was signif-
icantly lower (more than 10-fold and 2.8-fold lower than in the
control zone respectively) but a significant difference was no longer
observed after two years (Fig. 6). Infiltration rates, however, were

350
-

300 -
Macropore number (m-2)

250

200

150

100

50

0
0 5 10 15 20 25
Months after compaction

Fig. 3. Macropore number at each sampling date under wheel tracks (compacted) and between wheel tracks (control) for two pore size classes. For each class, differences between
compacted and control soil were significant except at the last sampling date (24 months after compaction).
 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103 99

Fig. 4. 3D reconstructions (after X-ray tomography) of the earthworm burrow systems inside soil cores (diameter ¼ 16 and length ¼ 40 cm) sampled under wheel tracks
(compacted) and between wheel tracks (control) one, 8 and 24 months after compaction. Colours range from yellow (front) and blue (back) to provide a 3D effect. (For interpretation
of the references to colour in this figure legend, the reader is referred to the web version of this article.)

very variable among dates for the control zones, ranging from 77 to
281 mm h
1.
4. Discussion
4.1. Soil compaction has immediate physical and biological effects
Soil compaction is a physical disturbance that generally causes
a decrease in soil porosity and thus an increase in bulk density,
which leads to unfavourable living conditions for soil organisms
(Beylich et al., 2010). Under the experimental conditions at the
Estrees-Mons site, the compaction event led to a significant
increase in the soil bulk density (1.57 g cm
3 under wheel tracks).
As shown by Schäffer et al. (2007), under these conditions macro-
pore number and continuity decreases. In our study, we observed
a significant decrease in macropore abundance at 10, 20 and 30 cm
depth with decreasing effects with depth (ranging from
70
to
30%) but no effect at 45 cm depth. The continuity of these
macropores was lower in the compacted zones as demonstrated by
the smaller proportion of coloured macropores at these three first
depths. These two observations are likely to explain the 90%
decrease in water infiltration, a value close to previous estimations
based on unsaturated hydraulic conductivity (Kim et al., 2010).
Earthworms are the soil organisms the most sensitive to soil
compaction (Althoff et al., 2009). We observed an initial and
significant decrease of 40% in the abundance of adults and 70% in
the total biomass. These values are in agreement with previous
studies (e.g. Cluzeau et al., 1992). When the effect is analysed
species by species, it appears that the mean abundance of
L. terrestris and A. rosea was lower, but not significantly, in com-
pacted zones than in control zones whereas this was not the case
for A. caliginosa (data not shown). Due to very high variability, it
was not possible to determine if compaction had a more significant
negative effect on adults than on juvenile earthworms as some-
times claimed (Cluzeau et al., 1992; Binet et al., 1997).
The decrease in earthworm abundance or biomass after soil
compaction is thought to have two origins: first the direct death of
animals by crushing (as observed during our first sampling) and
then the lateral escape of the surviving earthworms towards more
favourable conditions. In a recent experiment carried out to
100 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103

A 250
Volume of macroporosity

200
(cm3)

150

100

50

0
Control Compacted Control Compacted Control Compacted
M+1 (03/2005) M+8 (11/2005) M+24 (03/2007)

B 20
Fig. 6. Infiltration rates measured with the Beer-Kan method under wheel tracks
18
extension is greater than 5 cm

(compacted) and between wheel tracks (control). Stars indicate a significant difference
16 between compacted and control soil (each date was tested separately).
14
12
earthworms and increased earthworm biomass was observed in
10
the compacted zones as previously reported by Althoff et al. (2009)
8
in a tallgrass prairie compacted by tracked vehicles. Overall, our
6 results contrast greatly with previously published studies which
4 reported that earthworms were slow to recolonise compacted
2 zones in agricultural sites (Radford et al., 2001), forests (Ampoorter
0 et al., 2011) or during reclamation of open-cast mine sites (as
Control Compacted Control Compacted Control Compacted reviewed by Edwards and Bohlen, 1996) although in the last case,
M+1 (03/2005) M+8 (11/2005) M+24 (03/2007) compaction was not the only problem faced by earthworms. The
ability of earthworms to move vertically above the surface or
C underground is well known (Eijsackers, 2011) and they can move
100
rapidly to avoid unfavourable zones, for example after pesticide
is greater than 0.5 cm3

80 application (Christensen and Mather, 2004), to colonise reclaimed

polders (Ligthart and Peek, 1997) or higher quality habitats
60
(Mathieu et al., 2010) or during invasion processes (Daniel et al.,
1997).
40
The recolonisation of compacted soils by earthworms has been
20 studied mainly under laboratory conditions. Such studies demon-
strated that earthworms can recolonize compacted zones (Zund
0 et al., 1997; Langmaack et al., 1999; Jégou et al., 2002; Ponder
Control

Control

Control
Compacted

Compacted

Compacted

M+1 (03/2005)
Fig. 5. Some mean characteristics (and standard deviations) of the 3D burrow systems
from soil cores sampled nder wheel tracks (compacted, n ¼ 2) and between wheel
tracks (control, n ¼ 2): A ¼ total volume, B ¼ number of burrows whose vertical
extension was greater than 5 cm and C ¼ number of burrows whose volume was
greater than 0.5 cm3.
determine the physical resistance of A. caliginosa to physical stress
(high pressures), McKenzie et al. (2009) demonstrated that this
species is highly resistant and assumed that the decrease in
abundance observed under field conditions may be due mainly to
escape.
4.2. Rapid recolonisation of compacted zones by earthworms
It was surprising that the earthworms recolonised the com-
pacted zones so rapidly: three months after the compaction event,
earthworm abundance was no longer significantly different in the
compacted and non-compacted zones. Furthermore, after three
and nine months, a trend towards a greater number of adult
et al., 2000). However because they could not avoid these com-
pacted zones, these studies have led to a clear overestimation of
their role in soil regeneration as discussed by Langmaack et al.
M+8 (11/2005) M+24 (03/2007) (1999). In contrast, studies made under field or semi-field condi-
tions reached various conclusions. In the study by Radford et al.
(2007) earthworms did not recolonise the soil even after several
years. Capowiez et al. (2009b) observed limited recolonisation in
their short-term (two months) experiments. Larink and Schrader
(2000) reported a recovery under field conditions but no clear
indication of earthworm abundance or the time necessary to reach
recovery was given. Buckerfield and Wiseman (1997) found that
earthworm populations recovered quickly (after one year) after
heavily trafficked potato cropping compared to an adjacent pasture.
However, comparing all these field or semi-field studies remains
difficult since the experimental conditions (soil type, compaction
intensity, earthworm abundance) were different and as noticed by
Beylich et al. (2010), the precise experimental conditions were not
given in most cases.
Our findings thus raise the question of which specific factors in
our experimental conditions contributed to such a rapid recolo-
nisation of compacted zones by earthworms. The first factor could
be the spatial heterogeneity of the compaction at the plot scale.
Under our experimental conditions, the pattern of highly com-
pacted zones is representative of arable farming situations in
 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103
northern France: 36% of the soil surface was highly compacted and
the compacted zones corresponded to linear 0.55 m wide lanes
every 1.95 m. This means that the borders between compacted
and non-compacted zones were very large (1.43 m m
2 in
average). This may increase the probability of recolonisation
compared to homogeneously compacted rectangular plots
(Radford et al., 2001). Another factor could be that the experi-
mental plot in our case was superficially tilled. Furthermore,
a superficial tillage operation was carried out only two weeks after
the compaction event for seedbed preparation. This kind of tillage
created a top soil layer (with a mean depth of 7 cm) made of loose
soil. Thus it is possible that either, A. caliginosa (the most abundant
species in the compacted zones at least for the first dates) was able
to live and survive in such a thin soil layer, or this could have
enhanced earthworm lateral recolonisation and forced anecic
earthworms to burrow deeper in the compacted zones. In this
case, earthworm abundance is not a realistic reflection of efficient
soil regeneration, information on earthworm burrows and
possibly water infiltration is required.
4.3. Slower formation of macropores and thus slow recovery of
water infiltration
Formation of earthworm macropores, assessed in 2D, was much
slower than earthworm recolonisation and took between 12 and 24
months. This means that either macropore creation by each
earthworm in the compacted soil was reduced, as often observed
under laboratory conditions (Rushton, 1986; Kretzschmar, 1991;
Söchtig and Larink, 1992), or that an installed earthworm burrow
systems can be viewed as a balance between burrow creation (by
active earthworms) and burrow destruction (by earthworm refill-
ing or due to climatic conditions) as demonstrated by Ligthart
(1997). This suggests that more than one year might be necessary
to reach a steady state.
These 2D results were confirmed by our observations of the 3D
soil macroporosity for which we assume that the origin was mainly
earthworms (due to the tubular shapes and the diameter range).
The functional consequence of the recovery of the earthworm
burrow system was illustrated by the recovery of soil water infil-
tration indicating that both macropore density and continuity were
restored. The temporal scale used (only 1, 9 and 24 months after
compaction) prevented us from determining the recovery rate with
precision. However these overall observations are in agreement
with the results for 2D macroporosity and we can assume that
recovery was reached between 12 and 24 months.
In contrast, the structural porosity measured at a larger scale
(0.30 m wide and depth of 0.05e0.25 m) remained almost constant
two years after compaction, except for a small increase observed at
5e10 cm depth (Table 2). In another study conducted in the long-
term “Cropping systems and soil structure” experiment, we eval-
uated the recovery of structural porosity over a four year period in
a plot with the same soil texture. We observed that bulk density
remained very high, between 1.52 and 1.58 g cm
3, during the
following years, though there was no further severe compaction at
the time of field operations during the four year period (Roger-
Estrade et al., 2009). These results show that the time for
recovery depends greatly on the criteria under consideration: in
our case, earthworm abundance recovered within three months
after the compaction event, recolonisation by earthworm macro-
pores took between 12 and 24 months and the recovery of bulk
density took more than four years.
The scarcity of other studies of soil regeneration by earthworms
makes it difficult for us to compare the dynamics of this recovery
with previously published data. We could find only one reference
(Barros et al., 2001) that used soil blocks exchanged between
101
a pasture (compacted) and a forest (non-compacted) and deter-
mined that “one year was sufficient to transform the compact
structure of the pasture soil into a highly porous framework with
interconnected galleries”. However, we can expand our point of
view and take into account previous studies of soil recovery after
compaction that did not focus solely on the role of earthworms. For
example, based on macroporosity abundance, bulk density and
hydraulic properties, several authors (Douglas et al., 1998; McHugh
et al., 2009) found that the system recovered significantly 22 or 24
months after the compaction. These durations are indeed
in agreement with our observations of earthworm macropore
recolonisation. In contrast, Radford et al. (2007) found that soil
improvement after compaction, assessed through crop yield, water
storage and some physical parameters, can take five years. In that
study, it is possible that the low earthworm density (between
15 and 2 ind. m
2) found in the plots and the fact that entire
rectangular plots were compacted may have limited earthworm
recolonisation and thus earthworm contribution to soil
regeneration.
Even if, in our case, superficial tillage and the long border
between compacted and non-compacted soil may have facilitated
earthworm colonisation, the question remains why earthworms
burrowed in such dense soil layers implying a high energy cost. For
example, Larink and Schrader (2000) highlighted that earthworms
living in compacted plots have a lower individual biomass and
assumed this was due to a lower energy budget and thus more
energy needed for burrowing in the dense soils. In the Estrees-
Mons plots, earthworm abundance was relatively high for crop
conditions (about 100 ind. m
2 including adults and juveniles). This
could lead to high intra- and inter-specific competition between
earthworms for space and food (Uvarov, 2009) and thus may have
forced some earthworms to live under unfavourable conditions
(high bulk densities). Another reason could be that these com-
pacted zones may not represent permanently unfavourable
conditions. Indeed it is known that compacted zones become wet
more slowly than non-compacted zones but they also dry more
slowly during drought periods (Ampoorter et al., 2011). Thus
occasionally, active earthworms may find better humidity condi-
tions in the compacted zones.
5. Conclusions
Our results show that in silty soils earthworm populations do
contribute significantly to soil regeneration after compaction. After
a severe compaction, the number of macropores increased due to
earthworm activity in the highly compacted volumes but it took
more than two years for full recovery of burrow systems. The
infiltration rate, which was almost zero after compaction, increased
quickly after several months but it also took two years for it to fully
recover.
Despite this significant and rapid contribution of earthworms,
the soil structural porosity remained very low in compacted zones.
Other adverse consequences of compaction, which were not
studied in our experiment, such as shear strength and penetration
resistance, appear to have remained. Moreover, even if the field
conditions of this study are probably representative of a large area
in the Paris basin and northern France, our observations were made
at a single site and it is still possible that specific characteristics of
the soil (texture, hydraulic properties, pH.), climate or biology
(earthworm community, crops) influenced the speed at which the
earthworms were able to recolonise the compacted soil and thus
contribute to soil regeneration. More studies under various
edaphic, climatic and biological conditions are necessary to confirm
our results.
102 C. Yvan et al. / Soil Biology & Biochemistry 55 (2012) 93e103
Acknowledgements
This work was carried out with the financial support of the “ANR
e Agence Nationale de la Recherche e The French National
Research Agency” under the “Programme Agriculture et Dével-
oppement Durable”, “ANR-05-PADD-013, DST” and of the “MEDD e
The French Ministry of Environment and Sustainable Develop-
ment” under the “Programme Gessol2”. The authors are grateful for
the technical assistance of P. Regnier, B. Chauchard, the INRA
Domain for maintaining the long-term experiment. The Amiens
hospital is warmly thanked for kindly providing access to the
medical scanner.
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