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Interactions between earthworm species in artificial soil cores assessed through the 3D reconstruction of the burrow systems
Geoderma 102 Ž2001. 123–137 www.elsevier.nlrlocatergeoderma
Interactions between earthworm species in artificial soil cores assessed through the 3D reconstruction of the burrow systems Danielle Jegou ´ a,) , Yvan Capowiez b, Daniel Cluzeau a a
UniÕersite´ de Rennes 1, UMR A EcobioB , Laboratoire d’Ecologie du Sol et de Biologie des Populations, Station biologique, F-35380 Paimpont, France b INRA Zoologie, Domaine Saint Paul, F-84914 AÕignon cedex ´ 09, France
Received 2 November 1999; received in revised form 27 June 2000; received in revised form 6 November 2000; accepted 8 November 2000
Abstract The aim of this study was to determine the impact of the interactions between different earthworm species on the individual burrowing activity and especially on the characteristics of burrow systems. Towards this end, individuals of different earthworm species Ž Lumbricus terrestris, Aporrectodea giardi, A. caliginosa. were inoculated as single or paired species treatments into artificially packed soil columns. After 8 months, the soil columns were scanned by X-ray computed tomography. Three-dimensional skeletons of the burrow systems were then computed to characterise the burrow systems Žburrow number, total and mean burrowed length, segment distribution in relation to depth, and rate of branching.. Pronounced differences between species were found. L. terrestris built a permanent burrow system characterised by low burrowed length, few connections and low rate of branching. On the contrary, A. giardi and A. caliginosa dug temporary burrow systems. The burrow system of A. giardi was the most interconnected and showed the highest total and mean burrowed lengths. Differences observed between single and paired species treatments mainly concerned the distribution of the burrow system in relation to soil depth in the core and total burrowed length. The burrow system of L. terrestris was much less deep and showed a higher length when the species was incubated together with A. caliginosa. The burrow system of A. caliginosa was much deeper when the worm was cultivated with A. giardi. Differences in the rate of branching were
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Corresponding author. Fax: q33-2-99-61-81-87. E-mail address: [email protected] ŽD. Jegou ´ ..
0016-7061r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 1 6 - 7 0 6 1 Ž 0 0 . 0 0 1 0 7 - 5
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also shown in paired species treatments compared to single species treatments. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Earthworms; Lumbricus terrestris; Aporrectodea spp.; Species interaction; Burrow system; X-ray computed tomography
1. Introduction It is well known that the presence of earthworm burrows influence gas and water circulation in soil Ž Ehlers, 1975; Lopes-Assad, 1987; Joschko et al., 1989; Kretzschmar, 1989; Edwards et al., 1990; Urbanek and Dolezal, 1992. . The influence of burrow systems on these soil physical processes depends on their geometry and structural characteristics such as total burrowed length Ž Joschko et al., 1989., burrow diameter ŽLopes-Assad, 1987; Roth and Joschko, 1991. , continuity, interconnection between burrows and relationships with soil surface and soil matrix ŽBouma et al., 1982; West et al., 1991; Urbanek and Dolezal, 1992; Ligthart, 1996. . In spite of their importance, knowledge on burrow morphology is still limited. Moreover, available data are often qualitative. Field studies have shown that the burrow characteristics depend on abiotic parameters such as season Ž Kretzschmar, 1982; Capowiez et al., 1998. , soil compaction or tillage system Ž Langmaack et al., 1999. . Studies on individual earthworm species, which have generally been carried out in artificially compacted soil or in undisturbed soil monoliths, have shown that the burrow system has specific characteristics ŽJoschko et al., 1993; Jegou et al., 1998, 1999; ´ . Langmaack et al., 1999 . On the other hand, only few studies Ž Abbot, 1980; Hamilton et al., 1988; Elton and Koppi, 1994; Butt, 1998; Capowiez, 2000. consider the interactions between earthworms. For instance, interspecific relationships and their possible consequences on the individual burrowing activity have been neglected up to now. Thus, the aim of this study was to determine the impact of interactions between earthworm species of different morphoecological categories on the individual burrowing activity. With this end, the characteristics of the burrow systems of different species Ž total and mean burrowed length, segment distribution in relation to soil depth and rate of branching. have been compared in single and paired species treatments.
2. Material and methods In the field, it is difficult to link each species to a particular burrow structure and to compare individual burrowing activities at the same level of time and space. For these reasons, the study was carried out in an artificial system placed in laboratory.
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2.1. Experimental procedure Soil Ž21.4% clay, 68.2% silt and 10.4% sand; 0.4% organic matter; pH 6. , which was collected from the deep mineral horizon Ž between y70 and y80 cm depth. of a cultivated plot ŽBrittany, France. , was air-dried and sieved Ž- 2 mm.. After remoistening Ž20% dry weight 1058C., it was artificially compacted in polyvinyl chloride ŽP.V.C.. cylinders Ž 20 cm in diameter and 40 cm high. in six layers each to a bulk density of 1.35 g cmy3. The soil columns were then remoistened by capillary absorption and drained to reach a water potential of about 10 kPa ŽpF 2.. Adult individuals of earthworms were collected at the same plot as the soil: the epianecic Lumbricus terrestris L., the anecic Aporrectodea giardi ŽRibaucourt., and the endogeic A. caliginosa ŽSavigny. according to the ecological classification of Bouche´ Ž 1972. . Five treatments replicated three times were set up. Numbers and biomass of worms added were chosen to be close to field populations Ž Binet, 1993. : ŽA. ŽB. ŽC. ŽD. ŽE.
L. terrestris in single species treatment Ž two individuals. A. giardi in single species treatment Žtwo individuals. A. caliginosa in single species treatment Žsix individuals. L. terrestris Žone individual. and A. caliginosa Žthree individuals. A. giardi Žone individual. and A. caliginosa Žthree individuals..
The species and species combinations are commonly found in agroecosystems of Brittany. The food of earthworms consisted of dried ground litter of rye Ž 2.96% N and 42.07% C.. Based on data from literature ŽLee, 1985. , each microcosm received 0.011 g of litter per day per gram of introduced worm. The food was applied to the soil surface every 15 days. The microcosms were kept at 128C with 12 h light dayy1 for 246 days Žfrom the 15th of June to the 15th of February. . Fifty milliliter of distilled water was sprayed on the surface every 10 days. 2.2. Reconstruction and characterisation of the burrow systems At the end of the incubation, all columns were scanned by X-ray computed tomography ŽCT. at the University Hospital Centre of Pontchaillou Ž Rennes. , following the procedure described by Jegou et al. Ž 1998. . The CT unit was a ´ Siemens Somatom Plus. The columns were cut in a horizontal plane at 120 kV and 165 mA sy1. The slice thickness was 3 mm, which was sufficient to characterise the burrow systems of the three species studied Ž Jegou, 1998. . The ´ 3 voxel Ž volume element. size was 0.41 = 0.41 = 3 mm . Three-dimensional skeletons of the burrow systems were computed by the procedure used in Capowiez et al. Ž1998. , i.e. images were cleaned and then
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binarised using a simple algorithm: the binarisation threshold was set at a distance of 2r3 between the peak corresponding to the pores and that corresponding to the soil matrix. Pores related to earthworm activities were considered to have an area greater than 20 pixels Žthat corresponds to an equivalent circular diameter of 2 mm.. Pore continuity between slices was assessed following the overlap criterion of MacDonald et al. Ž 1986. : each object OŽ i . Žassumed to be an earthworm pore. of an image IŽ j . was projected onto the following image IŽ j q 1.. All pores of the images IŽ j q 1. that had at least one pixel in common with the projected object were considered to be connected to this object. Repeating this procedure between all successive images and drawing lines between centroids of all connected objects provided a skeleton reconstruction of the burrow system contained in the core. The connection between two objects belonging to two successive images was termed AsegmentB and sets of continuous segments was termed AburrowsB. The burrow system was the set of all the burrows contained in a core. The very short burrows which length was less than seven segments were removed. Using this method, it was then possible to compute several characteristics of the burrow systems. Some computed characteristics related to the entire burrow system: Ži. burrow number, Žii. total burrowed length, Žiii. burrow segment distribution with depth. Others focused more on the burrow itself : Ži. burrow mean length, Žii. rate of branching. The length of a burrow was set as the sum of the length of its constituent branches. The mean burrowed length was the total burrowed length divided by the number of burrows. Rate of branching was determined by counting the number of branches for all the burrows of a representative length Ž more than 20 segments. and by dividing this value by the total burrowed length. Due to differences in size of the earthworm species introduced in the paired species treatments Ž D and E., it was possible to separate the burrow systems in two sub-systems, one corresponding to each species. With this end, we studied the relation between the area of pores and the orientation of the segments for each core. We observed that the segment distributions of paired species treatments were clearly species specific. It was, however, impossible to determine the origin of the oblique segments, which could have been built by both species. Therefore, we decided to apply a partition in three areas: Ži. one in which segments probably belong to the smaller species Ž A. caliginosa.,
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Žii. another one in which segments probably belong to the larger species Ž A. giardi or L. terrestris ., Žiii. a last one, called Aneutral areaB, in which the probable origin of the segments could not be determined. This last area corresponds to oblique segments. The coordinates of the two points that determined the boundaries between the three areas were chosen using an optimisation procedure programmed with the Splus package ŽMathsoft. . The criteria for this optimisation procedure was the minimisation of the errors, i.e. percentage of segments from the single species treatments that were misclassified. The efficiency of this partition is as well assessed by the percentages of segments in the single species treatments that were misclassified Ži.e. the number of segments made by A. caliginosa that were in the area corresponding to the larger species and the number of segments made by A. giardi or L. terrestris that were in the area corresponding to the smaller species.. Means and confidence intervals Ž 0.05. Ž n s 3. were calculated for all the studied parameters. The paired species treatments contained twice as few individuals of the same species than the corresponding single species treatments. To allow comparisons between single and paired species treatments Ž Table 2. , the length of the total burrow system Ž values and confidence intervals. observed in the single species treatment was divided by 2. Using this method of calculation, we neglected intraspecific interactions and assumed that half of the individuals produced half of total burrowed length.
3. Results At the end of the experiment, all Ž in the case of epianecic and anecic species and in paired species treatments. or almost all Ž in the case of endogeic species. the litter had disappeared from the soil surface in all microcosms. The worms, which were extracted from the columns after the scanning procedure, were still alive and in most cases, a positive weight gain was observed. 3.1. Single species treatments The 3D skeleton reconstructions of burrow systems are shown in Fig. 1. Owing to the compaction procedure Ž by packing the cores with layers of soil of 3 and 5 cm., the upper part of each layer was slightly more dense than the rest of the soil, and boundaries between two successive layers were marked by a thin crack. The three species, especially L. terrestris and A. caliginosa, tended to follow this thin crack, so that the burrows were horizontal in these areas.
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Table 1 Characteristics of the single burrows and burrow systems in the single species treatments y1 .
Total burrowed length Žmm g worm Number of burrows per worm Mean length of burrow Žmm. Rate of branching Žm burrowy1 .
L. terrestris
A. giardi
A. caliginosa
439"238 7.5"5.2 216"25.9 2.6"0.3
2138"992 15.7"1.7 557"158.8 3.6"1
1590"830 10.4"2.4 74.4"38.6 2"1.6
Means and confidence intervals Ž0.05. Ž ns 3..
Table 1 shows characteristics wmeans and confidence intervals Ž 0.05.x of the single burrows and of the burrow systems in the single species treatments. The total burrowed length for A. giardi was about five times as long as for L. terrestris. The burrow length tended to be lower for L. terrestris compared to A.caliginosa. The number of burrows was the highest with A. giardi and the lowest with L. terrestris. The burrow system of A. caliginosa showed intermediate values for this parameter. The mean length of burrows was the highest with A. giardi and the lowest with A. caliginosa. The rate of branching tended to be higher with A. giardi compared to L. terrestris and A. caliginosa. 3.2. Comparing single and paired species treatments The distribution of the segments in the three defined areas Ž smaller species, larger species, neutral. gave satisfactory results as shown for A. caliginosa ŽFig. 2a. and A. giardi ŽFig. 2b.: the rates of segments from the single species treatment which are misclassified were only 7.5% for the cores incubated with A. caliginosa and 13.07% for the treatments incubated with L. terrestris and A. giardi. In all these cases, the segments from the neutral area represented less than 10% of the total number of segments. This discrimination enabled us to study in more detail the effect of the interactions on the burrowing activity of each species present in the mixed culture. Figs. 3, 4 and 5 show the burrow segment distribution in relation to the soil depth for each species in single and paired species treatments. In the case of L. terrestris Ž Fig. 3., the results showed that the burrow system was much deeper Ž200 to 280 mm. in the single species treatment than in the paired species treatment with A. caliginosa Žmax. 150 mm.. In this last case, the number of segments also tended to be higher in the first part of the column Ž up to 50 mm depth. than in the single species treatment. Those results are in accordance with 3D reconstructions of the burrow systems shown in Fig. 1. Fig. 1. 3D reconstructed skeletons of the burrow systems for one core incubated in single species treatment with L. terrestris Ža., A. giardi Žb., A. caliginosa Žc. and in mixed cultures with L. terrestris and A. caliginosa Žd., A. giardi and A. caliginosa Že..
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Fig. 2. Partition of the segments in relation to their area and their angle for one replicate of the treatments incubated with A. caliginosa Ža. and A. giardi Žb.. Area for the smaller species Ž1., area for the larger species Ž2. and neutral area Ž3..
The burrow system of A. caliginosa ŽFig. 4. was much deeper when the species was in the presence of A. giardi Ž240 to 280 mm. compared to the
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Fig. 3. Burrow system of L. terrestris —distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with A. caliginosa Žb..
Fig. 4. Burrow system of A. caliginosa—distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with L. terrestris Žb. or A. giardi Žc..
Fig. 5. Burrow system of A. giardi —distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with A. caliginosa Žb..
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Table 2 Length of the total burrow system Žmm. in the single and paired species treatments Treatments species
L. terrestris
A. giardi
A. caliginosa
L. terrestrisq A. caliginosa
A. giardiq A. caliginosa
L. terrestris A. giardi A. caliginosa Indeterminate
1558"898 – – –
– 8728"2753 – –
– – 2338"1457 –
3266"2070 – 3176"1029 y1143"889
– 4970"1665 2978"329 2339"1459
Means and confidence intervals Ž0.05. Ž ns 3.. The paired species treatments contained twice less individuals of the same species than the corresponding single species treatments. To allow comparisons between the two data sets, the length of the total burrow system Žvalues and confidence intervals. observed in the single species treatments ŽTable 1. were divided by two. AIndeterminateB corresponds to oblique burrow segments which were not related to a particular species.
single species treatment Žmax. 170 mm. or to the treatment where it is incubated with L. terrestris Žmax. 150 mm.. Finally, in this experiment, the burrowing activity of A. giardi Ž Fig. 5. seemed to be the less affected by species interactions: the burrow system always reached the bottom of the column. Nevertheless, there was a trend Ž two cores out of three. for this earthworm to have a greater number of segments in the upper part of the core when it was in presence of A. caliginosa, whereas in single species treatment, this species seemed to be more active in the middle of the core. Table 2 shows the length of the total burrow system for the different species in single and paired species treatments. The total burrowed length tended to be higher for L. terrestris when it was in presence of A. caliginosa compared to the single species treatment. On the contrary, the total length of the burrow system of A. giardi was twice less when it was cultivated with A. caliginosa compared to the single species treatment . Finally, the length of the burrow system of A. caliginosa was not significantly different in the presence of L.terrestris or A. giardi compared to the single species treatment.
Table 3 Characteristics of burrow systems observed in the paired species treatments
Total number of burrows Mean length of burrow Žmm. Rate of branching Žmy1 burrow.
L. terrestrisq A. caliginosa
A. giardiq A. caliginosa
38.7"26.8 145.7"70.8 3.3"0.3
75.3"7.9 143.1"66.4 4.2"0.3
Means and confidence intervals Ž0.05. Ž ns 3..
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The following results ŽTable 3. were obtained from data concerning the whole burrows in the columns, i.e. the different burrow systems were not separated to compute the characteristics that concern burrows. For the two paired treatments, the observed rate of branching was higher compared to the values obtained in the corresponding single species treatments ŽTable 1. . For the treatment containing A.giardi and A. caliginosa, the observed mean length of the burrow was very low compared to the value obtained for A. giardi in single species treatment.
4. Discussion 4.1. Single species treatments L. terrestris built a burrow system which was much shorter than that of the other anecic species, A. giardi. For two cores out of three, the network did not reach the bottom of the column. Burrows constitute a response to constraints Žfood supply, temperature, oxygen and water availability, . . . . encountered by earthworms in their environment Ž Kretzschmar, 1984. . In this study, the burrowing activity was located in the upper part of the soil column where favourable conditions, and especially food, were present. However, previous studies Ž Rogaar and Boswinkel, 1978; Lee, 1985. showed that, in the field, such a burrow system can extend to depths approaching 1 m and more. All the observed characteristics Žsmall total length, low rate of branching, . . . . confirmed previous findings based on qualitative or quantitative data obtained from artificial or semi-artificial conditions Ž Schrader et al., 1995; Jegou et al., 1998, 1999; ´ Langmaack et al., 1999. . The results allow to conclude that this species constructs a permanent burrow system, i.e. the worm always uses the same burrows. In accordance with the observations of Avel Ž 1929. , the burrowing activity of A. giardi was interrupted by a 2-month diapause Ž middle of June to middle of August.. This inactivity period was confirmed by a break in the feeding activity. In spite of this, the worm dug a complex burrow system showing a high number of burrows and an important burrowed length Ž five times more compared to L. terrestris .. The burrow system also tended to be characterised by a higher rate of branching compared to the other species. Taking into account the results obtained by Jegou et al. Ž1998, 1999., we can conclude that this network is ´ closer to the temporary burrow system described by Lee and Foster Ž 1991. for endogeic species than to the permanent burrow system of anecic species. For A. caliginosa, the maximal activity was in the top 7–8 cm, which could mean that, in this experiment, this endogeic species used surface litter as food source. This could be explained by the very low organic matter content of the
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soil used in the experiment. This assumption is in accordance with results obtained by Judas Ž 1992. showing that A. caliginosa can use different food sources. This result is also in agreement with field observations of McKenzie and Dexter Ž1993. who found the most complex region of the burrow network of A. caliginosa in the top 5 cm of the soil. The total burrowed length and the number of burrows were high but the rate of branching was low compared to the other species. 4.2. Comparing single and paired species treatments The comparison of the burrow system establishment in single and paired species treatments gave information about interactions between the studied species. In this experiment, there was no treatment containing only one individual. This means that the possible effects of intraspecific interactions on the individual burrowing activity cannot be assessed. In the case of L. terrestris, the results clearly showed that the burrow system was less deep when the worm was in presence of A. caliginosa than in the single species treatment. Moreover, the total burrowed length for L. terrestris tended to be higher in the paired species treatment than in the single one. As the organic matter content of the soil was very low Ž4 g kgy1 . , the litter deposited at the soil surface constituted a considerable source of organic matter in the system. Even if A. caliginosa clearly showed an epi-endogeic behaviour in this experiment, it consumed litter very slowly Ž Jegou, pers. obs.. . Therefore, in the ´ paired species treatment, the surface litter was available for L. terrestris, which tended to develop its burrow system at the top of the core. Elton and Koppi Ž1994., who analysed soil porosity in cores using Microscolex dubius and A. trapezoides in single and paired species treatments, showed that porosity was always greater when two species were incubated together with litter. In the present study, L. terrestris also burrowed a much more important length when it was cultivated with A. caliginosa. The burrow system of A. caliginosa was significantly deeper when it was in the presence of A. giardi compared to the single species treatment. Nevertheless, the burrowed length remained unchanged between the two treatments. The results may be explained in two ways. The first one is based on a competition for soil organic matter, the two species exploring the soil column throughout the whole depth searching for food. The second assumption is an interaction between the two species: A. caliginosa could use the burrow system of A. giardi to go deeper into the soil. Actually, Jegou et al. Ž 1998. showed that this ´ endogeic species is sensitive to variations in soil bulk densities due to the compaction procedure when producing artificial cores. Using the burrows dug by A. giardi could facilitate the movement through the core for A. caliginosa. Moreover, the burrow lining and the below ground casts of A. giardi, which are enriched with decomposed organic matter could constitute a food source for this
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endogeic species . This explanation is supported by the fact that the segment distribution of the burrow system of A. caliginosa ŽFig. 4c. tended to follow that observed for A. giardi ŽFig. 5b.. As the same was observed in the paired species treatment with L. terrestris, we can hypothesise that A. caliginosa needs foreign burrows or cracks to go deeper into the soil. Our experiment showed that species interaction can strongly influence the individual burrowing activity. The differences between the burrow system established in single and paired species treatments mainly concerned the spatial distribution in the core and the total burrowed length. Owing to experimental conditions and especially to the use of microcosms the observed burrowing behaviours may have been greatly amplified and simplified compared to field conditions. Nevertheless, our results can provide first explanations to understand the complex interspecific relationships existing between earthworms.
Acknowledgements This study was supported by the Conseil Regional de Bretagne and by the ´ Groupe Pluridisciplinaire Agrobiologie Bretagne Ž G.E.P.A.B.. . Pr. Gandon, B. Hervault and the scanner operators of the CHU of Pontchaillou Ž Rennes. are gratefully thanked for the opportunity of scanning the soil columns and for technical assistance. We thank Dr. M. Langmaack for his comments on the manuscript. Dr. S. Schrader and two other anonymous referees are acknowledged for their constructive help with our paper.
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natural earthworm burrow systems using CAT scan images of soil cores. Biol. Fertil. Soils 27, 51–59. Edwards, W.M., Shipitalo, M.J., Owens, L.B., Nortons, L.D., 1990. Effect of Lumbricus terrestris on hydrology of continuous no-till corn fields. Geoderma 46, 73–84. Ehlers, W., 1975. Observations on earthworm channels and infiltration on tilled and untilled loess soil. Soil Sci. 119, 242–249. Elton, K.L., Koppi, A.J., 1994. Image analysis of apedal soil following burrowing activity of Microscolex dubius ŽFletcher. and Aporrectodea trapezoides ŽDuges. ŽOligochaeta: Megascolidae Lumbricidae.. In: Pankhurst, C.E. ŽEd.., Colloquium Soil Biota: Management in Sustainable Farming Systems. CSIRO, Australia, pp. 132–136. Hamilton, W.E., Dindal, L.D., Parkinson, C.M., Mitchell, M.J., 1988. Interaction of earthworm species in sewage sludge-amended soil microcosms: Lumbricus terrestris and Eisenia fetida. J. Appl. Ecol. 25, 847–852. Jegou, D., 1998. Role ´ ˆ fonctionnel de quatre especes ` lombriciennes dans la structuration du sol et dans les transferts de carbone. PhD thesis, University of Rennes I, 146 pp. Jegou, D., Cluzeau, D., Wolf, H.J., Gandon, Y., Trehen, P., 1998. Assessment of the burrow ´ ´ system of Lumbricus terrestris, Aporrectodea giardi, and Aporrectodea caliginosa using X-ray computed tomography. Biol. Fertil. Soils 26, 116–121. Jegou, D., Hallaire, V., Cluzeau, D., Trehen, P., 1999. Characterisation of the burrow system of ´ ´ the earthworms Lumbricus terrestris and Aporrectodea giardi using X-ray computed tomography and image analysis. Biol. Fertil. Soils 29, 314–318. Joschko, M., Diestel, H., Larink, O., 1989. Assessment of earthworm burrowing efficiency in compacted soil with a combination of morphological and soil physical measurements. Biol. Fertil. Soils 8, 191–196. Joschko, M., Muller, P.C., Kotzke, K., Dohring, W., Larink, O., 1993. Earthworms burrow system ¨ development assessed by means of X-ray computed tomography. Geoderma 56, 209–221. Judas, M., 1992. Gut content analysis of earthworms ŽLumbricidae. in a beechwood. Soil Biol. Biochem. 24, 1413–1417. Kretzschmar, A., 1982. Elements de l’activite´ saisonniere ´ ` des vers de terre en prairie permanente. Rev. Ecol. Biol. Sol 19, 193–201. Kretzschmar, A., 1984. Besoins biologiques des vers de terre et porosite´ du sol. Bulletin du Groupe Franc¸ais d’Humidimetrie ´ et de tranferts en milieux poreux 15, 96–102. Kretzschmar, A., 1989. Galeries de lombriciens en reseaux: structures fonctionnelles et signatures ´ comportementales. These ` de l’universite´ de Paris Sud-centre d’Orsay, 228 pp. Langmaack, M., Schrader, S., Rapp-Bernhardt, U., Kotzke, K., 1999. Quantitative analysis of earthworm burrow system with respect to biological structure regeneration after soil compaction. Biol. Fertil. Soils 28, 219–229. Lee, K.E., 1985. Earthworms—Their Ecology and Relationships with Soils and Land Use. Academic Press, Sydney, 411 pp. Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Aust. J. Soil Res. 29, 745–775. Ligthart, T.N., 1996. Development of earthworm burrow systems and the influence of earthworms on soil hydrology. PhD thesis, University of Wageningen, 140 pp. Lopes-Assad, M.L., 1987. Contribution a` l’etude de la macroporosite´ lombricienne de differents ´ ´ types de sols en France. These ` de doctorat de l’universite´ de Montpellier, 218 pp. MacDonald, I., Kaufmann, P., Dullien, F., 1986. Quantitative image analysis of finite porous media: I. Development of genus and pore map software. J. Microsc. 144, 277–296. McKenzie, B.M., Dexter, A.R., 1993. Size and orientation of burrows made by the earthworms Aporrectodea rosea and Aporrectodea caliginosa. Geoderma 56, 233–241. Rogaar, H., Boswinkel, J.A., 1978. Some soil morphological effect of earthworm activity: field data and X-ray radiography. Neth. J. Agric. Sci. 26, 145–160.
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Interactions between earthworm species in artificial soil cores assessed through the 3D reconstruction of the burrow systems Danielle Jegou ´ a,) , Yvan Capowiez b, Daniel Cluzeau a a
UniÕersite´ de Rennes 1, UMR A EcobioB , Laboratoire d’Ecologie du Sol et de Biologie des Populations, Station biologique, F-35380 Paimpont, France b INRA Zoologie, Domaine Saint Paul, F-84914 AÕignon cedex ´ 09, France
Received 2 November 1999; received in revised form 27 June 2000; received in revised form 6 November 2000; accepted 8 November 2000
Abstract The aim of this study was to determine the impact of the interactions between different earthworm species on the individual burrowing activity and especially on the characteristics of burrow systems. Towards this end, individuals of different earthworm species Ž Lumbricus terrestris, Aporrectodea giardi, A. caliginosa. were inoculated as single or paired species treatments into artificially packed soil columns. After 8 months, the soil columns were scanned by X-ray computed tomography. Three-dimensional skeletons of the burrow systems were then computed to characterise the burrow systems Žburrow number, total and mean burrowed length, segment distribution in relation to depth, and rate of branching.. Pronounced differences between species were found. L. terrestris built a permanent burrow system characterised by low burrowed length, few connections and low rate of branching. On the contrary, A. giardi and A. caliginosa dug temporary burrow systems. The burrow system of A. giardi was the most interconnected and showed the highest total and mean burrowed lengths. Differences observed between single and paired species treatments mainly concerned the distribution of the burrow system in relation to soil depth in the core and total burrowed length. The burrow system of L. terrestris was much less deep and showed a higher length when the species was incubated together with A. caliginosa. The burrow system of A. caliginosa was much deeper when the worm was cultivated with A. giardi. Differences in the rate of branching were
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Corresponding author. Fax: q33-2-99-61-81-87. E-mail address: [email protected] ŽD. Jegou ´ ..
0016-7061r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 1 6 - 7 0 6 1 Ž 0 0 . 0 0 1 0 7 - 5
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also shown in paired species treatments compared to single species treatments. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Earthworms; Lumbricus terrestris; Aporrectodea spp.; Species interaction; Burrow system; X-ray computed tomography
1. Introduction It is well known that the presence of earthworm burrows influence gas and water circulation in soil Ž Ehlers, 1975; Lopes-Assad, 1987; Joschko et al., 1989; Kretzschmar, 1989; Edwards et al., 1990; Urbanek and Dolezal, 1992. . The influence of burrow systems on these soil physical processes depends on their geometry and structural characteristics such as total burrowed length Ž Joschko et al., 1989., burrow diameter ŽLopes-Assad, 1987; Roth and Joschko, 1991. , continuity, interconnection between burrows and relationships with soil surface and soil matrix ŽBouma et al., 1982; West et al., 1991; Urbanek and Dolezal, 1992; Ligthart, 1996. . In spite of their importance, knowledge on burrow morphology is still limited. Moreover, available data are often qualitative. Field studies have shown that the burrow characteristics depend on abiotic parameters such as season Ž Kretzschmar, 1982; Capowiez et al., 1998. , soil compaction or tillage system Ž Langmaack et al., 1999. . Studies on individual earthworm species, which have generally been carried out in artificially compacted soil or in undisturbed soil monoliths, have shown that the burrow system has specific characteristics ŽJoschko et al., 1993; Jegou et al., 1998, 1999; ´ . Langmaack et al., 1999 . On the other hand, only few studies Ž Abbot, 1980; Hamilton et al., 1988; Elton and Koppi, 1994; Butt, 1998; Capowiez, 2000. consider the interactions between earthworms. For instance, interspecific relationships and their possible consequences on the individual burrowing activity have been neglected up to now. Thus, the aim of this study was to determine the impact of interactions between earthworm species of different morphoecological categories on the individual burrowing activity. With this end, the characteristics of the burrow systems of different species Ž total and mean burrowed length, segment distribution in relation to soil depth and rate of branching. have been compared in single and paired species treatments.
2. Material and methods In the field, it is difficult to link each species to a particular burrow structure and to compare individual burrowing activities at the same level of time and space. For these reasons, the study was carried out in an artificial system placed in laboratory.
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2.1. Experimental procedure Soil Ž21.4% clay, 68.2% silt and 10.4% sand; 0.4% organic matter; pH 6. , which was collected from the deep mineral horizon Ž between y70 and y80 cm depth. of a cultivated plot ŽBrittany, France. , was air-dried and sieved Ž- 2 mm.. After remoistening Ž20% dry weight 1058C., it was artificially compacted in polyvinyl chloride ŽP.V.C.. cylinders Ž 20 cm in diameter and 40 cm high. in six layers each to a bulk density of 1.35 g cmy3. The soil columns were then remoistened by capillary absorption and drained to reach a water potential of about 10 kPa ŽpF 2.. Adult individuals of earthworms were collected at the same plot as the soil: the epianecic Lumbricus terrestris L., the anecic Aporrectodea giardi ŽRibaucourt., and the endogeic A. caliginosa ŽSavigny. according to the ecological classification of Bouche´ Ž 1972. . Five treatments replicated three times were set up. Numbers and biomass of worms added were chosen to be close to field populations Ž Binet, 1993. : ŽA. ŽB. ŽC. ŽD. ŽE.
L. terrestris in single species treatment Ž two individuals. A. giardi in single species treatment Žtwo individuals. A. caliginosa in single species treatment Žsix individuals. L. terrestris Žone individual. and A. caliginosa Žthree individuals. A. giardi Žone individual. and A. caliginosa Žthree individuals..
The species and species combinations are commonly found in agroecosystems of Brittany. The food of earthworms consisted of dried ground litter of rye Ž 2.96% N and 42.07% C.. Based on data from literature ŽLee, 1985. , each microcosm received 0.011 g of litter per day per gram of introduced worm. The food was applied to the soil surface every 15 days. The microcosms were kept at 128C with 12 h light dayy1 for 246 days Žfrom the 15th of June to the 15th of February. . Fifty milliliter of distilled water was sprayed on the surface every 10 days. 2.2. Reconstruction and characterisation of the burrow systems At the end of the incubation, all columns were scanned by X-ray computed tomography ŽCT. at the University Hospital Centre of Pontchaillou Ž Rennes. , following the procedure described by Jegou et al. Ž 1998. . The CT unit was a ´ Siemens Somatom Plus. The columns were cut in a horizontal plane at 120 kV and 165 mA sy1. The slice thickness was 3 mm, which was sufficient to characterise the burrow systems of the three species studied Ž Jegou, 1998. . The ´ 3 voxel Ž volume element. size was 0.41 = 0.41 = 3 mm . Three-dimensional skeletons of the burrow systems were computed by the procedure used in Capowiez et al. Ž1998. , i.e. images were cleaned and then
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binarised using a simple algorithm: the binarisation threshold was set at a distance of 2r3 between the peak corresponding to the pores and that corresponding to the soil matrix. Pores related to earthworm activities were considered to have an area greater than 20 pixels Žthat corresponds to an equivalent circular diameter of 2 mm.. Pore continuity between slices was assessed following the overlap criterion of MacDonald et al. Ž 1986. : each object OŽ i . Žassumed to be an earthworm pore. of an image IŽ j . was projected onto the following image IŽ j q 1.. All pores of the images IŽ j q 1. that had at least one pixel in common with the projected object were considered to be connected to this object. Repeating this procedure between all successive images and drawing lines between centroids of all connected objects provided a skeleton reconstruction of the burrow system contained in the core. The connection between two objects belonging to two successive images was termed AsegmentB and sets of continuous segments was termed AburrowsB. The burrow system was the set of all the burrows contained in a core. The very short burrows which length was less than seven segments were removed. Using this method, it was then possible to compute several characteristics of the burrow systems. Some computed characteristics related to the entire burrow system: Ži. burrow number, Žii. total burrowed length, Žiii. burrow segment distribution with depth. Others focused more on the burrow itself : Ži. burrow mean length, Žii. rate of branching. The length of a burrow was set as the sum of the length of its constituent branches. The mean burrowed length was the total burrowed length divided by the number of burrows. Rate of branching was determined by counting the number of branches for all the burrows of a representative length Ž more than 20 segments. and by dividing this value by the total burrowed length. Due to differences in size of the earthworm species introduced in the paired species treatments Ž D and E., it was possible to separate the burrow systems in two sub-systems, one corresponding to each species. With this end, we studied the relation between the area of pores and the orientation of the segments for each core. We observed that the segment distributions of paired species treatments were clearly species specific. It was, however, impossible to determine the origin of the oblique segments, which could have been built by both species. Therefore, we decided to apply a partition in three areas: Ži. one in which segments probably belong to the smaller species Ž A. caliginosa.,
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Žii. another one in which segments probably belong to the larger species Ž A. giardi or L. terrestris ., Žiii. a last one, called Aneutral areaB, in which the probable origin of the segments could not be determined. This last area corresponds to oblique segments. The coordinates of the two points that determined the boundaries between the three areas were chosen using an optimisation procedure programmed with the Splus package ŽMathsoft. . The criteria for this optimisation procedure was the minimisation of the errors, i.e. percentage of segments from the single species treatments that were misclassified. The efficiency of this partition is as well assessed by the percentages of segments in the single species treatments that were misclassified Ži.e. the number of segments made by A. caliginosa that were in the area corresponding to the larger species and the number of segments made by A. giardi or L. terrestris that were in the area corresponding to the smaller species.. Means and confidence intervals Ž 0.05. Ž n s 3. were calculated for all the studied parameters. The paired species treatments contained twice as few individuals of the same species than the corresponding single species treatments. To allow comparisons between single and paired species treatments Ž Table 2. , the length of the total burrow system Ž values and confidence intervals. observed in the single species treatment was divided by 2. Using this method of calculation, we neglected intraspecific interactions and assumed that half of the individuals produced half of total burrowed length.
3. Results At the end of the experiment, all Ž in the case of epianecic and anecic species and in paired species treatments. or almost all Ž in the case of endogeic species. the litter had disappeared from the soil surface in all microcosms. The worms, which were extracted from the columns after the scanning procedure, were still alive and in most cases, a positive weight gain was observed. 3.1. Single species treatments The 3D skeleton reconstructions of burrow systems are shown in Fig. 1. Owing to the compaction procedure Ž by packing the cores with layers of soil of 3 and 5 cm., the upper part of each layer was slightly more dense than the rest of the soil, and boundaries between two successive layers were marked by a thin crack. The three species, especially L. terrestris and A. caliginosa, tended to follow this thin crack, so that the burrows were horizontal in these areas.
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Table 1 Characteristics of the single burrows and burrow systems in the single species treatments y1 .
Total burrowed length Žmm g worm Number of burrows per worm Mean length of burrow Žmm. Rate of branching Žm burrowy1 .
L. terrestris
A. giardi
A. caliginosa
439"238 7.5"5.2 216"25.9 2.6"0.3
2138"992 15.7"1.7 557"158.8 3.6"1
1590"830 10.4"2.4 74.4"38.6 2"1.6
Means and confidence intervals Ž0.05. Ž ns 3..
Table 1 shows characteristics wmeans and confidence intervals Ž 0.05.x of the single burrows and of the burrow systems in the single species treatments. The total burrowed length for A. giardi was about five times as long as for L. terrestris. The burrow length tended to be lower for L. terrestris compared to A.caliginosa. The number of burrows was the highest with A. giardi and the lowest with L. terrestris. The burrow system of A. caliginosa showed intermediate values for this parameter. The mean length of burrows was the highest with A. giardi and the lowest with A. caliginosa. The rate of branching tended to be higher with A. giardi compared to L. terrestris and A. caliginosa. 3.2. Comparing single and paired species treatments The distribution of the segments in the three defined areas Ž smaller species, larger species, neutral. gave satisfactory results as shown for A. caliginosa ŽFig. 2a. and A. giardi ŽFig. 2b.: the rates of segments from the single species treatment which are misclassified were only 7.5% for the cores incubated with A. caliginosa and 13.07% for the treatments incubated with L. terrestris and A. giardi. In all these cases, the segments from the neutral area represented less than 10% of the total number of segments. This discrimination enabled us to study in more detail the effect of the interactions on the burrowing activity of each species present in the mixed culture. Figs. 3, 4 and 5 show the burrow segment distribution in relation to the soil depth for each species in single and paired species treatments. In the case of L. terrestris Ž Fig. 3., the results showed that the burrow system was much deeper Ž200 to 280 mm. in the single species treatment than in the paired species treatment with A. caliginosa Žmax. 150 mm.. In this last case, the number of segments also tended to be higher in the first part of the column Ž up to 50 mm depth. than in the single species treatment. Those results are in accordance with 3D reconstructions of the burrow systems shown in Fig. 1. Fig. 1. 3D reconstructed skeletons of the burrow systems for one core incubated in single species treatment with L. terrestris Ža., A. giardi Žb., A. caliginosa Žc. and in mixed cultures with L. terrestris and A. caliginosa Žd., A. giardi and A. caliginosa Že..
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Fig. 2. Partition of the segments in relation to their area and their angle for one replicate of the treatments incubated with A. caliginosa Ža. and A. giardi Žb.. Area for the smaller species Ž1., area for the larger species Ž2. and neutral area Ž3..
The burrow system of A. caliginosa ŽFig. 4. was much deeper when the species was in the presence of A. giardi Ž240 to 280 mm. compared to the
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Fig. 3. Burrow system of L. terrestris —distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with A. caliginosa Žb..
Fig. 4. Burrow system of A. caliginosa—distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with L. terrestris Žb. or A. giardi Žc..
Fig. 5. Burrow system of A. giardi —distribution of the segment number in relation to the soil depth in single species treatment Ža. and in paired species culture with A. caliginosa Žb..
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Table 2 Length of the total burrow system Žmm. in the single and paired species treatments Treatments species
L. terrestris
A. giardi
A. caliginosa
L. terrestrisq A. caliginosa
A. giardiq A. caliginosa
L. terrestris A. giardi A. caliginosa Indeterminate
1558"898 – – –
– 8728"2753 – –
– – 2338"1457 –
3266"2070 – 3176"1029 y1143"889
– 4970"1665 2978"329 2339"1459
Means and confidence intervals Ž0.05. Ž ns 3.. The paired species treatments contained twice less individuals of the same species than the corresponding single species treatments. To allow comparisons between the two data sets, the length of the total burrow system Žvalues and confidence intervals. observed in the single species treatments ŽTable 1. were divided by two. AIndeterminateB corresponds to oblique burrow segments which were not related to a particular species.
single species treatment Žmax. 170 mm. or to the treatment where it is incubated with L. terrestris Žmax. 150 mm.. Finally, in this experiment, the burrowing activity of A. giardi Ž Fig. 5. seemed to be the less affected by species interactions: the burrow system always reached the bottom of the column. Nevertheless, there was a trend Ž two cores out of three. for this earthworm to have a greater number of segments in the upper part of the core when it was in presence of A. caliginosa, whereas in single species treatment, this species seemed to be more active in the middle of the core. Table 2 shows the length of the total burrow system for the different species in single and paired species treatments. The total burrowed length tended to be higher for L. terrestris when it was in presence of A. caliginosa compared to the single species treatment. On the contrary, the total length of the burrow system of A. giardi was twice less when it was cultivated with A. caliginosa compared to the single species treatment . Finally, the length of the burrow system of A. caliginosa was not significantly different in the presence of L.terrestris or A. giardi compared to the single species treatment.
Table 3 Characteristics of burrow systems observed in the paired species treatments
Total number of burrows Mean length of burrow Žmm. Rate of branching Žmy1 burrow.
L. terrestrisq A. caliginosa
A. giardiq A. caliginosa
38.7"26.8 145.7"70.8 3.3"0.3
75.3"7.9 143.1"66.4 4.2"0.3
Means and confidence intervals Ž0.05. Ž ns 3..
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The following results ŽTable 3. were obtained from data concerning the whole burrows in the columns, i.e. the different burrow systems were not separated to compute the characteristics that concern burrows. For the two paired treatments, the observed rate of branching was higher compared to the values obtained in the corresponding single species treatments ŽTable 1. . For the treatment containing A.giardi and A. caliginosa, the observed mean length of the burrow was very low compared to the value obtained for A. giardi in single species treatment.
4. Discussion 4.1. Single species treatments L. terrestris built a burrow system which was much shorter than that of the other anecic species, A. giardi. For two cores out of three, the network did not reach the bottom of the column. Burrows constitute a response to constraints Žfood supply, temperature, oxygen and water availability, . . . . encountered by earthworms in their environment Ž Kretzschmar, 1984. . In this study, the burrowing activity was located in the upper part of the soil column where favourable conditions, and especially food, were present. However, previous studies Ž Rogaar and Boswinkel, 1978; Lee, 1985. showed that, in the field, such a burrow system can extend to depths approaching 1 m and more. All the observed characteristics Žsmall total length, low rate of branching, . . . . confirmed previous findings based on qualitative or quantitative data obtained from artificial or semi-artificial conditions Ž Schrader et al., 1995; Jegou et al., 1998, 1999; ´ Langmaack et al., 1999. . The results allow to conclude that this species constructs a permanent burrow system, i.e. the worm always uses the same burrows. In accordance with the observations of Avel Ž 1929. , the burrowing activity of A. giardi was interrupted by a 2-month diapause Ž middle of June to middle of August.. This inactivity period was confirmed by a break in the feeding activity. In spite of this, the worm dug a complex burrow system showing a high number of burrows and an important burrowed length Ž five times more compared to L. terrestris .. The burrow system also tended to be characterised by a higher rate of branching compared to the other species. Taking into account the results obtained by Jegou et al. Ž1998, 1999., we can conclude that this network is ´ closer to the temporary burrow system described by Lee and Foster Ž 1991. for endogeic species than to the permanent burrow system of anecic species. For A. caliginosa, the maximal activity was in the top 7–8 cm, which could mean that, in this experiment, this endogeic species used surface litter as food source. This could be explained by the very low organic matter content of the
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soil used in the experiment. This assumption is in accordance with results obtained by Judas Ž 1992. showing that A. caliginosa can use different food sources. This result is also in agreement with field observations of McKenzie and Dexter Ž1993. who found the most complex region of the burrow network of A. caliginosa in the top 5 cm of the soil. The total burrowed length and the number of burrows were high but the rate of branching was low compared to the other species. 4.2. Comparing single and paired species treatments The comparison of the burrow system establishment in single and paired species treatments gave information about interactions between the studied species. In this experiment, there was no treatment containing only one individual. This means that the possible effects of intraspecific interactions on the individual burrowing activity cannot be assessed. In the case of L. terrestris, the results clearly showed that the burrow system was less deep when the worm was in presence of A. caliginosa than in the single species treatment. Moreover, the total burrowed length for L. terrestris tended to be higher in the paired species treatment than in the single one. As the organic matter content of the soil was very low Ž4 g kgy1 . , the litter deposited at the soil surface constituted a considerable source of organic matter in the system. Even if A. caliginosa clearly showed an epi-endogeic behaviour in this experiment, it consumed litter very slowly Ž Jegou, pers. obs.. . Therefore, in the ´ paired species treatment, the surface litter was available for L. terrestris, which tended to develop its burrow system at the top of the core. Elton and Koppi Ž1994., who analysed soil porosity in cores using Microscolex dubius and A. trapezoides in single and paired species treatments, showed that porosity was always greater when two species were incubated together with litter. In the present study, L. terrestris also burrowed a much more important length when it was cultivated with A. caliginosa. The burrow system of A. caliginosa was significantly deeper when it was in the presence of A. giardi compared to the single species treatment. Nevertheless, the burrowed length remained unchanged between the two treatments. The results may be explained in two ways. The first one is based on a competition for soil organic matter, the two species exploring the soil column throughout the whole depth searching for food. The second assumption is an interaction between the two species: A. caliginosa could use the burrow system of A. giardi to go deeper into the soil. Actually, Jegou et al. Ž 1998. showed that this ´ endogeic species is sensitive to variations in soil bulk densities due to the compaction procedure when producing artificial cores. Using the burrows dug by A. giardi could facilitate the movement through the core for A. caliginosa. Moreover, the burrow lining and the below ground casts of A. giardi, which are enriched with decomposed organic matter could constitute a food source for this
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endogeic species . This explanation is supported by the fact that the segment distribution of the burrow system of A. caliginosa ŽFig. 4c. tended to follow that observed for A. giardi ŽFig. 5b.. As the same was observed in the paired species treatment with L. terrestris, we can hypothesise that A. caliginosa needs foreign burrows or cracks to go deeper into the soil. Our experiment showed that species interaction can strongly influence the individual burrowing activity. The differences between the burrow system established in single and paired species treatments mainly concerned the spatial distribution in the core and the total burrowed length. Owing to experimental conditions and especially to the use of microcosms the observed burrowing behaviours may have been greatly amplified and simplified compared to field conditions. Nevertheless, our results can provide first explanations to understand the complex interspecific relationships existing between earthworms.
Acknowledgements This study was supported by the Conseil Regional de Bretagne and by the ´ Groupe Pluridisciplinaire Agrobiologie Bretagne Ž G.E.P.A.B.. . Pr. Gandon, B. Hervault and the scanner operators of the CHU of Pontchaillou Ž Rennes. are gratefully thanked for the opportunity of scanning the soil columns and for technical assistance. We thank Dr. M. Langmaack for his comments on the manuscript. Dr. S. Schrader and two other anonymous referees are acknowledged for their constructive help with our paper.
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