Y. Capowiez et al. Applied Soil Ecology 16 2001 109–120 115
Fig. 3. Distributions of segments in the plane defined by the seg- ment angle and the minimum area of the two pores at the extrem-
ities of each segment: A — burrow system made by A. nocturna in the core 001; B — burrow system made by A. chlorotica in
the core 004; C — boundaries of the separation 1 and 2: parts where the segments were probably made by A. chlorotica and A.
nocturna, respectively; 3: ‘neutral zone’.
3.4. Diffusion measurements Soil diffusion coefficients were of the same magni-
tude in all the cores. In the first set of measurements, we observed that these coefficients were significantly
larger for the cores that contained both species of earthworms P = 0.03; Table 4. Unfortunately this
trend was not found in the second repetition P = 0.15; Table 4.The continuity was lower in the cores
that contained A. chlorotica T2 whatever the number of virtual planes Fig. 5. No difference was observed
between the T1 and the T3 cores.
4. Discussion
4.1. Differences between the burrow systems Horizontal burrows were absent from our artifi-
cial cores in contrast to similar experiments using the same method Jégou et al., 1998. This indicates
that our protocol based on relatively small soil layers and surface scratching is satisfactory and prevents
earthworms from burrowing horizontally between the artificial soil layers. However, this method still suffers
from spatial limitations. This is evidenced by the ex- istence of a border effect we found a greater number
of burrows near the walls of the cores which was greater for A. nocturna T1 than for A. chlorotica
T2 results not shown.
The burrow systems of the two species studied are clearly different and these differences are in
agreement with the postulated characteristics of bur- row systems from endogeic and anecic species Lee
and Foster, 1991. The burrows made by the anecic species were more vertical, longer, less branched and
less sinuous than those made by the endogeic species. These characteristics have consequences for burrow
system continuity with A. nocturna burrows being more continuous than those of A. chlorotica. In spite
of these differences, no difference was found in gas relative diffusivity coefficients for the burrow systems
made by the two species.
In a previous study using 2D terraria Capowiez, 2000 very few differences were found in the shape
of the burrow systems of these two species but this was probably due to the high spatial limitations en-
116 Y. Capowiez et al. Applied Soil Ecology 16 2001 109–120
Table 3 Comparisons of the characteritics of the burrow systems of each species after the separation only the characteristics for which a difference
was observed are presented A. nocturna
A. chlorotica T1 n = 2
T3 n = 3 T2 n = 3
T3 n = 3 Total length m per earthworm
1.98 1.21
1.13 0.61
1.50 0.57
1.21 0.63
1.26 1.66
1.21 Number of burrows per earthworm
12.2 8
6.5 3
8 13.2
17.2 15
16.7 18.5
17.5 Segment mean angular deviation
◦
33.5 35.0
31.5 33.1
29.5 39.3
41.8 38.5
39.8 43.2
42.2 Mean burrow length mm
387 278
160 124
173 73
133 70
111 98
105 Rate of burrow branching m
− 1
11.3 11.9
28.3 26.1
33.4 31.8
27.0 35.1
19.4 30.5
13.7
Fig. 4. Mean number of segments made by one species at an increasing distance from the segments made by the other species K-functions: solid line is the distribution for the observed core and dotted lines indicates the hull of the distributions for the 24 simulated cores. See
text for further explanations.
Y. Capowiez et al. Applied Soil Ecology 16 2001 109–120 117
Table 4 Diffusion coefficients 10
− 5
m
2
s
− 1
for the 10 studied cores
a
A. nocturna A. chlorotica
Both species P
001 002
003 004
005 006
007 008
009 010
0.848 0.671
0.826 0.856
0.726 0.853
0.896 0.894
0.872 0.922
0.030 0.884
0.665 0.838
0.904 0.757
0.792 0.885
0.907 0.845
1.000 0.153
a
The P-value of the Kruskall Wallis test is given for the two repetitions.
countered by the earthworms in these very artificial conditions. In the 2D terraria the behaviour of these
two species was very different: the anecic species of- ten reused their burrows and the endogeic species
rarely did so. Three-dimensional reconstructions and 2D terraria, therefore, give us complementary results.
While other authors have already noted these profound differences in the shape of the burrow systems between
the two ecological types Evans, 1947; Jégou et al., 1998, these previous studies were not able to quan-
tify the observed structures. We believe that 3D skele- ton reconstructions is a tool that allows us to move
beyond the descriptive stage of earthworm ecology Curry, 1998. Other methods using X-ray tomogra-
phy are available, such as the volume reconstructions developed by Langmaack et al. 1999. This method
presents interesting characterisations such as burrow
Fig. 5. Continuity of the eight burrow systems assessed by counting the number of different pathways that linked artificial equidistant horizontal planes.
volumes but computations of burrow lengths are not straightforward.
It is possible to compare 3D reconstructions from these artificial cores with 3D reconstructions from nat-
ural cores obtained from a pre-alpine meadow where A. nocturna was the dominant species Capowiez et al.,
1998; Capowiez et al., in press. These comparisons show that burrows in artificial cores are much longer
and more branched. Besides, the total burrow length is greater in artificial cores: it ranges from 2.8 to 5 m
in natural cores whereas it ranges from 3.6 to 7.6 m in artificial cores in this case only the first 20 cm
are considered. As it can be assumed that the bio- logical erosion of burrows through backfilling with
casts is the same in the two cases, these differences illustrate the importance of physical erosion of bur-
rows through trampling for example under natural
118 Y. Capowiez et al. Applied Soil Ecology 16 2001 109–120
conditions. Moreover, in artificial cores the burrows are recent the experiment lasted only 2 months and
therefore they are well preserved even in the case of endogeic burrows that are generally thought to be
more ‘labile’ in natural conditions since they are rarely reused Capowiez, 2000.
4.2. Interspecific interaction in T3 To assign segments in the burrow systems from
cores of T3 to each species, a criterium based on differ- ences between earthworm diameters is used, but this
criterium alone is not sufficient to ensure efficient sep- aration. Knowledge of the 3D structure of the burrow
system enables us i to modulate this criterium by the orientation of segments and ii to propose corrections
based on continuity properties of burrows. Finally this separation is characterized by a mean error rate of
only 10. This is the first time, to our knowledge, that such a clear separation is proposed and obtained. It
represents an interesting advance that could help us in studying complex natural burrow systems. Moreover,
this separation allows the study of modifications of the burrow system of each species due to the presence of
the other species. In our study, the structure of the bur- row systems elaborated by A. nocturna is greatly in-
fluenced by the presence of A. chlorotica: A. nocturna made less burrows which were more vertical, smaller
and less branched. Conversely A. chlorotica exhibits no significant modification in the structure of its bur-
row system. These results contrast greatly with our previous study using 2D terraria where we observed
that the behaviour of A. chlorotica was negatively in- fluenced by the presence of A. nocturna these earth-
worms made shorter burrows and explored a smaller surface and that the presence of A. chlorotica had
no effect on the behaviour of A. nocturna. Interac- tions between earthworm species have not been exten-
sively studied Curry, 1998, and the main focus was often the effects of such interactions on growth or re-
productive output Abbott, 1980; Elvira et al., 1996; Butt, 1998. To our knowledge, the work of Elton and
Koppi 1994 with Microscolex dubius and Aporrec- todea trapezoides is the only previous study that takes
the burrowing behaviour of the earthworm species into account. These authors showed that burrow length was
always greater when only one species was present. The major difficulty in this kind of experiment focusing on
interactions between species, assessed by observation of modifications in the structure of the burrow sys-
tems, is that the direction and the nature of the possi- ble interactions are ignored Capowiez et al., in press.
Moreover, in this experiment, the effect of interspe- cific interactions is intimately tied with a decrease in
intraspecific interactions the number of earthworms of each species in T3 is only half than in T1 or T2. To
gain insight into these interactions, it would be nec- essary to study the possible trophic interactions be-
tween these two species. Indeed, some authors have suggested that endogeic species could feed on the casts
of anecic species Shaw and Pawluk, 1986; Bouché, 1987; Bernier, 1998. More studies on these relation-
ships are required to obtain a clear picture from the results presented. At this stage, it is still impossible
to say whether these interactions are linked to spatial competition or to trophic interactions competition or
mutualism for example between earthworm species.
Burrow systems made by the two species together in the same cores T3 tend to be the most efficient for
gas diffusion. These results cannot be explained by the total burrow length of these burrow systems no sig-
nificant correlation was found or by burrow system continuity T1 cores were found to be as continuous as
T3 cores. Further studies are needed to better under- stand the relationship between soil diffusion improve-
ment and the characteristics of the burrow systems.
5. Conclusions
