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Distribution and abundance of burrows formed by Lumbricus terrestris L. and Aporrectodea caliginosa Sav. in the soil profile
Soil Biol. Biochem. Vol. 29, No. 3/4, pp. 463-467, 1997 0 1997 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0038-0717/97 $17.00 + 0.00
PII: soo38-0717(%)ooo&5
DISTRIBUTION AND ABUNDANCE OF BURROWS FORMED BY LUMBRICUS TERRESTRIS L. AND APORRECTODEA CALIGINOSA SAV. IN THE SOIL PROFILE JYRKI
and VISA NUUTINEN2t
PITKANENl*
‘Agricultural Research Centre, Institute of Crop and Soil Science, FIN-31608 Jokioinen, Finland and ‘University of Joensuu, Department of Biology, P.O. Box 111, FIN-80101 Joensuu, Finland (Accepted I2 March 1996)
Sumsnary-The distribution of burrows made by Lumbricus terrestris L. and Aporrectodea caliginosa Sav. was studied on an unploughed field. The positions of earthworm burrows were mapped in 9 horizontal planes to a depth of 80 cm in a pit of 70 by 40 cm. Burrow diameter and presence of plant roots growing in burrows were also recorded. Burrows on six of the nine planes were considered as twodimensional point patterns and analyzed as spatial point processes. A three-dimensional image was constructed for burrows formed by L. terrestris. The total number of burrows ranged between 180 and 1260 m-’ at depths of 80 and 30 cm, respectively. The majority of burrows were evidently formed by A. caliginosa. The smallest size class (2-3 mm) of burrows was dominant at depths between 8 and 40 cm. Deeper in the soil profile, the proportion of larger burrows increased markedly. Burrows formed by L. terrestris appeared to be non-branching, and extended vertically beyond 80 cm. In all soil layers studied, burrow distribution was found to be completely random. The proportion of burrows containing plant roots was between 18 and 60%, at depths of 80 and 15 cm, respectively. 0 1997 Elsevier Science Ltd
INTRODUCIION
three-dimensional burrow structure expressed as volume or length fraction of the profile (We&l, 1979). The main objective of our study was to investigate the spatial distribution of earthworm burrows, at different soil depths, by excavation and mapping in the field.
Use of morphological measurements to characterize earthworm burrow features is important in order to understand their significance for different soil processes, such as water and gas transport (Bouma, 1990; Smettem, 1992). Several studies have reported on the numbers of earthworm burrows per unit area, as well as the diameter and continuity of these burrows (Ehlers, 1975; Barnes and Ellis, 1979; Shipitalo and Protz, 1987; Edwards et al., 1988; Logsdon et al., 1990). Three-dimensional representations of burrows have been produced by using different excavation techniques (Kretzschmar, 1978; Joschko et al., 1992; Ligthart et al., 1993; McKenzie and Dexter, 1993). Studying two-dimensional spatial patterns of earthworm burrows measured in cross-sections provides information on amount and structure of soil utilization by earthworms. So far, only a few attempts have been made towards modeling burrow distributions (Smettem and Collis-George, 1985; Kretzschmar, 1987; Haukka, 1991). Further, stereological considerations can be applied to cross-sectional data in order to derive characteristics of the
MATERIALS AND METHODS
*Corresponding author. tPresent address: Agricultural Research Centre, Institute of Crop and Soil Science. FIN-31600 Jokioinen, Finland.
The site was a field experimental plot in Jokioinen, southern Finland (60”49’N; 23”28’E), where reduced tillage on spring cereal cultivation is studied (Pitklnen, 1993). The soil type is a clay soil with 42% clay, 39% silt and 19% sand (Soil Survey Staff, 1975). The plot studied had been under reduced tillage since 1979. Tillage was restricted to seedbed preparation in spring with a s-tine harrow to a depth of 5 cm. Every year crop residues were left on the soil surface after harvest. A combined seed and fertilizer drill (12.5 cm seedrow spacing) was used for sowing. A compound fertilizer (N-PK) was placed between every other seedrow to a depth of 8-10 cm. From earthworm sampling conducted on site in 1987-1988, only two species were found present, Aporrectodea caliginosa Sav., a subsurface dweller and feeder, and Lumbricus terrestris L., a deep-burrowing surface feeder (Nuutinen, 1992). These two species are usually the most common earthworms found in arable Finnish soils.
463
464
Jyrki Pitklnen and Visa Nuutinen
The study was conducted between mid-July and mid-August, 1993. The growing season had been dry, and soil moisture was low at the beginning of the excavation. One pit of size 100 by 60 cm was the focus of investigation. Vegetation (spring oats) was removed from the studied area, and the soil surface was examined for earthworm burrows opening to the surface. All surface-open burrows found were individually stained with methylene blue before excavation was begun. To avoid effects of soil deformation near the pit walls, the actual mapping area was reduced to 70 by 40 cm located in the center of the larger area. However, the surface-open and continuous ( = stained) burrows were recorded for the larger area of 100 by 60 cm. The mapping procedure was modified from that used by McKenzie and Dexter (1993). A metal framework was fixed on the soil surface, and the position of burrows was determined with a pointer moving in x, y and z directions. Burrow mapping was made in 9 horizontal planes ranging from the soil surface to a depth of 80 cm. Only burrows with dia 22 mm were included. Burrow sizes of 2-3. 3-5 and > 5 mm were recorded and presence of plant roots in these burrows was noted. Roots growing in the soil matrix or along ped faces were not recorded. At the soil surface and second soil layer (5cm depth) only stained burrows were mapped due to difficulties in preparing the crumbly top soil. At the third layer (IO-cm depth), mapping was partly hindered by the large abundance of oat roots, consequently studied area was restricted to 45 by 40 cm at this depth. Rains in mid-August filled the monitoring pit with water, and brought an end to the study at a depth of 80 cm. Earthworms were hand sorted from the 70 by 40 cm area in each of seven soil layers as excavation proceeded (Table 1.) L. terrestris were extracted individually from their burrows with dilute formalin at a depth of 60 cm. Extraction of L. terrestris included the wider area where the stained burrows were followed. Collected earthworms were stored in alcohol, and later identified to species. Dry weights of worms, which include the gut contents, were measured after approximately 12 h at 105°C. Burrow area, as a proportion of the total, was calculated from the average diameter of the two smallest size classes (2.5 and 4 mm), and the lower
size limit for the largest size class (5 mm) at each depth studied. Percent area was then converted to volume fraction of burrows according to the basic equation of stereology, area fraction = volume fraction (Weibel, 1979). Three-dimensional images were re-constructed for active, stained, surface-open burrows (i.e. burrows which contained an individual L. terrestris).
The pattern of burrows at the six deepest soil layers. where the data was suitable for the analysis. was studied using second order analysis of point processes based on Ripley’s K-function (Ripley, 198 1). This is defined as follows: K(r) = A-’ EJN(r)], where f$N(r)] is the expected number of further burrows within a circle of radius r around a randomly chosen burrow, and 1 is the mean number of burrows per unit area. If the distribution of burrows is completely random, corresponding to the Poisson distribution, then K(r) = nr* for all distances r. In order to simplify the interpretation of the K-function, a transformed version L(r) = J[K(r)/n] is used. In the case of the L(r) = r for all distances r. LPoisson distribution, function values where L(r) > r indicate aggregation (burrows tend to be closer to one another than expected in a random pattern), and values where L(r) < r indicate regularity (burrows tend to be be farther away from one another than expected in a random pattern). The L-function can be estimated from the mapped pattern of burrows using edge correction [for details, see Ripley (1981)]. The pointwise confidence bounds can be found by applying the simulation based formula +I .IS,/(area/n) of Ripley (1988), where n is the number of observations.
RESULTS
Total number of burrows ranged between 178 and 1264 m-* and volume fraction between 0.22 and 1.03% at depths of 80 and 30 cm, respectively (Fig. 1). The smallest size class of burrows was dominant at depths between 8 and 40 cm (median size class = 2-3 mm). Deeper in the soil profile, the proportion of larger burrows increased markedly (median size class = 3-5 mm). The proportion of burrows containing plant roots was between 18 and 60%, at depths of 80 and 15 cm, respectively (Fig. 2, see also Fig. 3). The per-
Table 1. Number (no. m-2) and dry weight (dwt g m-‘) of handsorted earthworms at the studied 70 by 40 cm area, the average dry weight (dwt g) of A. caliainosa and the proportion (%) of juvenile A. cafi~inosa in different soil layers
Layer (cm) O-8 8-15 15-20 20-30 30-40 40-60 60-80
Number (no. m-*) 104 82 50 II 0 0 0
Total dwt (g mm*) 1.25 1.71 2.18 0.43 0 0 0
Average dwt of Ax. (mg) (SE) 12 21 44 40
(2) (4) (4) (6)
Proportion of juvenile Ax. (%) 88 78 33 0
465
Distribution and abundance of earthworm burrows Volume fraction 0.0
0
0.4
0.2
I
0.6
(%) 0.8
/
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/
10 20 P
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40
c?
50 60 70 80 I-0
4 0
200
400
600
800
1000
1200
1400
40
20
60
80
100
Burrows with roots (“IO)
No. of burrows m-* t t t A
2-3 3-5 a5
mm mm mm
t
All burrows
Fig. 1. The number (no. m-*) of earthworm burrows of different sizes and their fraction of the soil volume (%) at
different depths on the studied 70 by 40cm area. At the soil surface and second soil layer (S-cm depth) only stained burrows were mapped. At the depth of 1Ocm the studied area was restricted to 45 by 40 cm.
3-5
mm
+>5mm
Fig. 2. The proportion (%) of earthworm burrows of different size containing plant roots at different soil layers on the area of 70 by 40 cm. The presence of roots was not recorded at the soil surface and at depths of 5 and 10 cm.
smaller than those found deeper in the soil. All A. caliginosa were quiescent and curled into aestivation chambers.
DISCUSSION
centage of burrows containing roots was usually smallest in size class 2-3 mm, and largest in burrows > 5 mm. A number of A. caliginosa burrows ended in an aestivation chamber, and often a dense coil of roots was found in the chamber. Burrow distribution and L(r)-function, at a depth of 30 cm, are shown in Figs 3 and 4 as an example of mapping data. The L(r)-function remains within the 95% confidence limits (Fig. 4), which indicates random distribution of burrows at all distances. Similarly, the distribution of burrows was found to be random at all other soil layers. Within the area of 100 by 60 cm, there were 11 burrows open to the soil surface. These stained burrows continued almost vertically to a depth greater than 80 cm. All but two contained an individual L. terrestris (Fig. 5). Only four of the 9 active L. terrestris burrows were within the 70 by 40cm area studied. Plant roots were observed to grow to a depth of 60 cm in the L. terrestris burrows. Of the handsorted earthworms, all were A. caliginosa except for one small juvenile L. terrestris found in the first soil layer. The number of individuals decreased with increasing soil depth. The last A. caliginosa were found in the 20 to 30-cm layer (Table 1). Close to the soil surface, a larger proportion of individuals were juveniles, and they were
Tillage has a strong effect on earthworm burrowing activity due to relocation of organic material and changing soil temperature and moisture gradients. Tillage also destroys earthworm burrows (Edwards, 1983). The shallow tillage of our study distributes crop residues fairly evenly in the top layer of soil, and the damaging effect of tillage implements on burrows is restricted to approximately 5 cm deep. This kind of soil management may contribute to the observed non-aggregated pattern of burrows in the soil profile. Our results agree with observations of Smettem and Collis-George (1985),
Fig. 3. The distribution of earthworm burrows (> 2 mm) at a depth of 30cm. Open circles: burrows with no roots; filled circles: burrows with roots.
Jyrki Pitkanen and Visa Nuutinen
466
who reported random distribution of earthworm burrows for a long-term pasture soil. Under more intensive and deeper tillage, the pattern of earthworm burrows may be different, due to uneven residue placement and strongly altered soil physical environment. Haukka (1991) studied the pattern of earthworm burrows from soil samples, and observed that 9 of 10 analyzed patterns were aggregated in distances larger than 31 mm. Both tilled and untilled soils were studied, but it was not evident which tillage treatments and soil layers were included in analysis. The majority of burrows smaller than 5 mm were evidently formed by A. caliginosa. The larger median size of burrows in the two deepest soil layers was presumably due to the fact that the activity of small A. caliginosa occurred primarily in the top soil. There were many apparent A. caliginosa burrows below the depth where aestivating individuals were found. It is possible that these burrows are formed during the winter, if A. caliginosa burrows deeper to escape frost than summer droughts. It is hard to evaluate the importance of the high density of A. caliginosa burrows on different soil processes, because of the lack of burrow length and orientation measurements. However, A. caliginosa burrows can be relatively continuous, and contribute to water movement in soil. McKenzie and Dexter (1993) found that the average length of A. rosea and A. caliginosa burrows was 39.2 cm, and that these burrows were orientated horizontally near the soil surface, but more vertically with increasing depth. Joschko et nl. (1992) observed that the saturated hydraulic conductivity was positively correlated with the length of A. caliginosa burrows.
a-
0
2
4
6
8
20 g
40 60 80 0
20
Fig. 5. Three-dimensional illustration of active L. rerresrris burrows at the 100 by 60 cm area.
The surface opening and continuous burrows of L. terrestris are considered to be important channels for preferential flow of water and solutes (Ehlers, 1975; Edwards et al., 1990). At the field scale, distribution of L. terrestris may vary considerably (Poier and Richter, 1992). This may also be the case at a small scale. However, because of the small number of observations, no definite conclusions on the small scale pattern of L. terrestris burrows can be drawn from this study. Earthworm burrows were frequently used as passage ways by plant roots. In the subsoil, with high penetration resistance, all root growth may be restricted to these continuous burrows (Bohm and Kopke, 1977; Ehlers et al., 1983). In addition to burrows of L. terrestris, burrows formed by large, adult A. caliginosa may also be more continuous and reach deeper soil layers than burrows made by juveniles and small adults. Therefore, the observation that the proportion of burrows containing roots was highest in large burrows may indicate preferable continuity and orientation of these burrows for root growth. Excavation and mapping in the field proved to be a useful, although time consuming, technique in Further earthworm burrow and root studies. research is needed to discover the pattern of burrows formed by L. terrestris, and the possible variation in burrow distribution in differently tilled soils. Also, the interaction between burrows, plant roots and other macropores needs more detailed research.
10
Distance (cm) Fig. 4. Ripley’s K-function (L-transformation) for the burrow distribution at a depth of 3Ocrn. Dashed lines: 95% confidence limits.
Acknowledgements-We thank Dr Antti Penttinen for his statistical consultation, Dr Kevin Butt and two anonymous referees for their comments on the manuscript, and Taisto Siren and Ari Pdyhiinen for their technical assistance.
461
Distribution and abundance of earthworm burrows REFERENCES
Barnes B.T. and Ellis F.B. (1979) Effects of different methods of cultivation and direct drilling, and disposal of straw residues, on populations of earthworms. Journal of Soil Science 30, 6699679. Bouma J. (1990) Using morphometric expressions for macropores to improve soil physical analyses of field soils. Geoderma 46, 3-l I. Biihm W. and Kiipke U. (1977) Comparative root investigations with two profile wall methods. Zeitschrif fiir Acker- und Pflanzenbau 144, 297-303. Edwards, C. A. (1983) Earthworm ecology in cultivated soils. In Earthworm Ecology (J. E. Satchell, Ed.), pp. 123-137. Chapman and Hall, London. Edwards W.M., Norton L.D. and Redmond C.E. (1988) Characterizing macropores that affect infiltration into non-tilled soil. Soil Science Society of America Journal 52, 483-487.
Edwards W.M., Shipitalo M.J., Owens L.B. and Norton L.D. (1990) Effect of Lumbricus terrestris L. burrows 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 Science 119, 242-249.
Ehlers W., Klipke U., Hesse F. and Bohm W. (1983) Penetration resistance and root growth of oats in tilled and untilled loess soil. Soil & Tillage Research 3, 26l275.
Haukka J. (1991) Spatial distribution and formation of earthworm burrows Pedobiologia 35, 175-178. Joschko M.. Siichtia W. and Larink 0. (1992) Functional relationship between earthworm burrows and soil water movement in column experiments. Soil Biology and Biochemistry 24, 1545-1547. Kretzschmar A. (1978) Quantification ecologique des galeries de lombriciens. Techniques et premieres estimations. Pedobiologia 18, 31-38. Kretzschmar A. (1987) Soil partitioning effect of an earthworm burrow system. Biology and Fertility of Soils 3, 121-124.
Ligthart T.N., Peek G.J.W.C. and Taber E.J. (1993) A method for the three-dimensional mapping of earthworm burrow systems. Geoderma 57, 1299141. Logsdon S.D., Allmaras R.R., Wu L., Swan J.B. and Randall G.W. (1990) Macroporosity and its relation to saturated hydraulic conductivity under different tillage practices. Soil Science Society of America Journal 54, 1096-l 101.
McKenzie B.M. and Dexter A.R. (1993) Size and orientation of burrows made by the earthworms Aporrectodea rosea and A. caliginosa. Geoderma 56, 233-241.
Nuutinen V. (1992) Earthworm community response to tillage and residue management on different soil types in southern Finland. Soil & Tillage Research 23. 221-239. Pitklnen J. (1993) The effects of-tillage and straw management on earthworm burrows in soil. Nordiska Jordbruksforskares 301-306.
Ftirening.
UtredningjRapport
88,
Poier K.R. and Richter J. (1992) Spatial distribution of earthworms and soil properties in an arable loess soil. Soil Biology and Biochemistry 24, 1601-1608.
Ripley, B. D. (1981) Spatial Statistics. John Wiley & Sons, New York. Ripley, B. D. (1988) Statistical Inference /or Spatial Processes. Cambridge University Press, Cambridge. Shipitalo M.J. and Protz R. (1987) Comparison of morphology and porosity of a soil under conventional and zero tillage. Canadian Journal of Soil Science 67, 445456.
Smettem K.R.J. (1992) The relation of earthworms to soil hydraulic properties. Soil Biology and Biochemistry 24, 1539-1543.
Smettem K.R.J. and Collis-George N. (1985) Statistical characterization of soil biopores using a soil peel method. Geoderma 36, 27-36. Soil Survey Staff (1975) Soil taxonomy. United States Department of Agriculture, Soil Conservation Service, Agricultural Handbook No. 436. U.S. Government Printing Office, Washington, DC. Weibel, E. R. (1979) Stereological Methods, Vol. I. Academic Press, London.
PII: soo38-0717(%)ooo&5
DISTRIBUTION AND ABUNDANCE OF BURROWS FORMED BY LUMBRICUS TERRESTRIS L. AND APORRECTODEA CALIGINOSA SAV. IN THE SOIL PROFILE JYRKI
and VISA NUUTINEN2t
PITKANENl*
‘Agricultural Research Centre, Institute of Crop and Soil Science, FIN-31608 Jokioinen, Finland and ‘University of Joensuu, Department of Biology, P.O. Box 111, FIN-80101 Joensuu, Finland (Accepted I2 March 1996)
Sumsnary-The distribution of burrows made by Lumbricus terrestris L. and Aporrectodea caliginosa Sav. was studied on an unploughed field. The positions of earthworm burrows were mapped in 9 horizontal planes to a depth of 80 cm in a pit of 70 by 40 cm. Burrow diameter and presence of plant roots growing in burrows were also recorded. Burrows on six of the nine planes were considered as twodimensional point patterns and analyzed as spatial point processes. A three-dimensional image was constructed for burrows formed by L. terrestris. The total number of burrows ranged between 180 and 1260 m-’ at depths of 80 and 30 cm, respectively. The majority of burrows were evidently formed by A. caliginosa. The smallest size class (2-3 mm) of burrows was dominant at depths between 8 and 40 cm. Deeper in the soil profile, the proportion of larger burrows increased markedly. Burrows formed by L. terrestris appeared to be non-branching, and extended vertically beyond 80 cm. In all soil layers studied, burrow distribution was found to be completely random. The proportion of burrows containing plant roots was between 18 and 60%, at depths of 80 and 15 cm, respectively. 0 1997 Elsevier Science Ltd
INTRODUCIION
three-dimensional burrow structure expressed as volume or length fraction of the profile (We&l, 1979). The main objective of our study was to investigate the spatial distribution of earthworm burrows, at different soil depths, by excavation and mapping in the field.
Use of morphological measurements to characterize earthworm burrow features is important in order to understand their significance for different soil processes, such as water and gas transport (Bouma, 1990; Smettem, 1992). Several studies have reported on the numbers of earthworm burrows per unit area, as well as the diameter and continuity of these burrows (Ehlers, 1975; Barnes and Ellis, 1979; Shipitalo and Protz, 1987; Edwards et al., 1988; Logsdon et al., 1990). Three-dimensional representations of burrows have been produced by using different excavation techniques (Kretzschmar, 1978; Joschko et al., 1992; Ligthart et al., 1993; McKenzie and Dexter, 1993). Studying two-dimensional spatial patterns of earthworm burrows measured in cross-sections provides information on amount and structure of soil utilization by earthworms. So far, only a few attempts have been made towards modeling burrow distributions (Smettem and Collis-George, 1985; Kretzschmar, 1987; Haukka, 1991). Further, stereological considerations can be applied to cross-sectional data in order to derive characteristics of the
MATERIALS AND METHODS
*Corresponding author. tPresent address: Agricultural Research Centre, Institute of Crop and Soil Science. FIN-31600 Jokioinen, Finland.
The site was a field experimental plot in Jokioinen, southern Finland (60”49’N; 23”28’E), where reduced tillage on spring cereal cultivation is studied (Pitklnen, 1993). The soil type is a clay soil with 42% clay, 39% silt and 19% sand (Soil Survey Staff, 1975). The plot studied had been under reduced tillage since 1979. Tillage was restricted to seedbed preparation in spring with a s-tine harrow to a depth of 5 cm. Every year crop residues were left on the soil surface after harvest. A combined seed and fertilizer drill (12.5 cm seedrow spacing) was used for sowing. A compound fertilizer (N-PK) was placed between every other seedrow to a depth of 8-10 cm. From earthworm sampling conducted on site in 1987-1988, only two species were found present, Aporrectodea caliginosa Sav., a subsurface dweller and feeder, and Lumbricus terrestris L., a deep-burrowing surface feeder (Nuutinen, 1992). These two species are usually the most common earthworms found in arable Finnish soils.
463
464
Jyrki Pitklnen and Visa Nuutinen
The study was conducted between mid-July and mid-August, 1993. The growing season had been dry, and soil moisture was low at the beginning of the excavation. One pit of size 100 by 60 cm was the focus of investigation. Vegetation (spring oats) was removed from the studied area, and the soil surface was examined for earthworm burrows opening to the surface. All surface-open burrows found were individually stained with methylene blue before excavation was begun. To avoid effects of soil deformation near the pit walls, the actual mapping area was reduced to 70 by 40 cm located in the center of the larger area. However, the surface-open and continuous ( = stained) burrows were recorded for the larger area of 100 by 60 cm. The mapping procedure was modified from that used by McKenzie and Dexter (1993). A metal framework was fixed on the soil surface, and the position of burrows was determined with a pointer moving in x, y and z directions. Burrow mapping was made in 9 horizontal planes ranging from the soil surface to a depth of 80 cm. Only burrows with dia 22 mm were included. Burrow sizes of 2-3. 3-5 and > 5 mm were recorded and presence of plant roots in these burrows was noted. Roots growing in the soil matrix or along ped faces were not recorded. At the soil surface and second soil layer (5cm depth) only stained burrows were mapped due to difficulties in preparing the crumbly top soil. At the third layer (IO-cm depth), mapping was partly hindered by the large abundance of oat roots, consequently studied area was restricted to 45 by 40 cm at this depth. Rains in mid-August filled the monitoring pit with water, and brought an end to the study at a depth of 80 cm. Earthworms were hand sorted from the 70 by 40 cm area in each of seven soil layers as excavation proceeded (Table 1.) L. terrestris were extracted individually from their burrows with dilute formalin at a depth of 60 cm. Extraction of L. terrestris included the wider area where the stained burrows were followed. Collected earthworms were stored in alcohol, and later identified to species. Dry weights of worms, which include the gut contents, were measured after approximately 12 h at 105°C. Burrow area, as a proportion of the total, was calculated from the average diameter of the two smallest size classes (2.5 and 4 mm), and the lower
size limit for the largest size class (5 mm) at each depth studied. Percent area was then converted to volume fraction of burrows according to the basic equation of stereology, area fraction = volume fraction (Weibel, 1979). Three-dimensional images were re-constructed for active, stained, surface-open burrows (i.e. burrows which contained an individual L. terrestris).
The pattern of burrows at the six deepest soil layers. where the data was suitable for the analysis. was studied using second order analysis of point processes based on Ripley’s K-function (Ripley, 198 1). This is defined as follows: K(r) = A-’ EJN(r)], where f$N(r)] is the expected number of further burrows within a circle of radius r around a randomly chosen burrow, and 1 is the mean number of burrows per unit area. If the distribution of burrows is completely random, corresponding to the Poisson distribution, then K(r) = nr* for all distances r. In order to simplify the interpretation of the K-function, a transformed version L(r) = J[K(r)/n] is used. In the case of the L(r) = r for all distances r. LPoisson distribution, function values where L(r) > r indicate aggregation (burrows tend to be closer to one another than expected in a random pattern), and values where L(r) < r indicate regularity (burrows tend to be be farther away from one another than expected in a random pattern). The L-function can be estimated from the mapped pattern of burrows using edge correction [for details, see Ripley (1981)]. The pointwise confidence bounds can be found by applying the simulation based formula +I .IS,/(area/n) of Ripley (1988), where n is the number of observations.
RESULTS
Total number of burrows ranged between 178 and 1264 m-* and volume fraction between 0.22 and 1.03% at depths of 80 and 30 cm, respectively (Fig. 1). The smallest size class of burrows was dominant at depths between 8 and 40 cm (median size class = 2-3 mm). Deeper in the soil profile, the proportion of larger burrows increased markedly (median size class = 3-5 mm). The proportion of burrows containing plant roots was between 18 and 60%, at depths of 80 and 15 cm, respectively (Fig. 2, see also Fig. 3). The per-
Table 1. Number (no. m-2) and dry weight (dwt g m-‘) of handsorted earthworms at the studied 70 by 40 cm area, the average dry weight (dwt g) of A. caliainosa and the proportion (%) of juvenile A. cafi~inosa in different soil layers
Layer (cm) O-8 8-15 15-20 20-30 30-40 40-60 60-80
Number (no. m-*) 104 82 50 II 0 0 0
Total dwt (g mm*) 1.25 1.71 2.18 0.43 0 0 0
Average dwt of Ax. (mg) (SE) 12 21 44 40
(2) (4) (4) (6)
Proportion of juvenile Ax. (%) 88 78 33 0
465
Distribution and abundance of earthworm burrows Volume fraction 0.0
0
0.4
0.2
I
0.6
(%) 0.8
/
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/
10 20 P
30
Y r z
40
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No. of burrows m-* t t t A
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mm mm mm
t
All burrows
Fig. 1. The number (no. m-*) of earthworm burrows of different sizes and their fraction of the soil volume (%) at
different depths on the studied 70 by 40cm area. At the soil surface and second soil layer (S-cm depth) only stained burrows were mapped. At the depth of 1Ocm the studied area was restricted to 45 by 40 cm.
3-5
mm
+>5mm
Fig. 2. The proportion (%) of earthworm burrows of different size containing plant roots at different soil layers on the area of 70 by 40 cm. The presence of roots was not recorded at the soil surface and at depths of 5 and 10 cm.
smaller than those found deeper in the soil. All A. caliginosa were quiescent and curled into aestivation chambers.
DISCUSSION
centage of burrows containing roots was usually smallest in size class 2-3 mm, and largest in burrows > 5 mm. A number of A. caliginosa burrows ended in an aestivation chamber, and often a dense coil of roots was found in the chamber. Burrow distribution and L(r)-function, at a depth of 30 cm, are shown in Figs 3 and 4 as an example of mapping data. The L(r)-function remains within the 95% confidence limits (Fig. 4), which indicates random distribution of burrows at all distances. Similarly, the distribution of burrows was found to be random at all other soil layers. Within the area of 100 by 60 cm, there were 11 burrows open to the soil surface. These stained burrows continued almost vertically to a depth greater than 80 cm. All but two contained an individual L. terrestris (Fig. 5). Only four of the 9 active L. terrestris burrows were within the 70 by 40cm area studied. Plant roots were observed to grow to a depth of 60 cm in the L. terrestris burrows. Of the handsorted earthworms, all were A. caliginosa except for one small juvenile L. terrestris found in the first soil layer. The number of individuals decreased with increasing soil depth. The last A. caliginosa were found in the 20 to 30-cm layer (Table 1). Close to the soil surface, a larger proportion of individuals were juveniles, and they were
Tillage has a strong effect on earthworm burrowing activity due to relocation of organic material and changing soil temperature and moisture gradients. Tillage also destroys earthworm burrows (Edwards, 1983). The shallow tillage of our study distributes crop residues fairly evenly in the top layer of soil, and the damaging effect of tillage implements on burrows is restricted to approximately 5 cm deep. This kind of soil management may contribute to the observed non-aggregated pattern of burrows in the soil profile. Our results agree with observations of Smettem and Collis-George (1985),
Fig. 3. The distribution of earthworm burrows (> 2 mm) at a depth of 30cm. Open circles: burrows with no roots; filled circles: burrows with roots.
Jyrki Pitkanen and Visa Nuutinen
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who reported random distribution of earthworm burrows for a long-term pasture soil. Under more intensive and deeper tillage, the pattern of earthworm burrows may be different, due to uneven residue placement and strongly altered soil physical environment. Haukka (1991) studied the pattern of earthworm burrows from soil samples, and observed that 9 of 10 analyzed patterns were aggregated in distances larger than 31 mm. Both tilled and untilled soils were studied, but it was not evident which tillage treatments and soil layers were included in analysis. The majority of burrows smaller than 5 mm were evidently formed by A. caliginosa. The larger median size of burrows in the two deepest soil layers was presumably due to the fact that the activity of small A. caliginosa occurred primarily in the top soil. There were many apparent A. caliginosa burrows below the depth where aestivating individuals were found. It is possible that these burrows are formed during the winter, if A. caliginosa burrows deeper to escape frost than summer droughts. It is hard to evaluate the importance of the high density of A. caliginosa burrows on different soil processes, because of the lack of burrow length and orientation measurements. However, A. caliginosa burrows can be relatively continuous, and contribute to water movement in soil. McKenzie and Dexter (1993) found that the average length of A. rosea and A. caliginosa burrows was 39.2 cm, and that these burrows were orientated horizontally near the soil surface, but more vertically with increasing depth. Joschko et nl. (1992) observed that the saturated hydraulic conductivity was positively correlated with the length of A. caliginosa burrows.
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Fig. 5. Three-dimensional illustration of active L. rerresrris burrows at the 100 by 60 cm area.
The surface opening and continuous burrows of L. terrestris are considered to be important channels for preferential flow of water and solutes (Ehlers, 1975; Edwards et al., 1990). At the field scale, distribution of L. terrestris may vary considerably (Poier and Richter, 1992). This may also be the case at a small scale. However, because of the small number of observations, no definite conclusions on the small scale pattern of L. terrestris burrows can be drawn from this study. Earthworm burrows were frequently used as passage ways by plant roots. In the subsoil, with high penetration resistance, all root growth may be restricted to these continuous burrows (Bohm and Kopke, 1977; Ehlers et al., 1983). In addition to burrows of L. terrestris, burrows formed by large, adult A. caliginosa may also be more continuous and reach deeper soil layers than burrows made by juveniles and small adults. Therefore, the observation that the proportion of burrows containing roots was highest in large burrows may indicate preferable continuity and orientation of these burrows for root growth. Excavation and mapping in the field proved to be a useful, although time consuming, technique in Further earthworm burrow and root studies. research is needed to discover the pattern of burrows formed by L. terrestris, and the possible variation in burrow distribution in differently tilled soils. Also, the interaction between burrows, plant roots and other macropores needs more detailed research.
10
Distance (cm) Fig. 4. Ripley’s K-function (L-transformation) for the burrow distribution at a depth of 3Ocrn. Dashed lines: 95% confidence limits.
Acknowledgements-We thank Dr Antti Penttinen for his statistical consultation, Dr Kevin Butt and two anonymous referees for their comments on the manuscript, and Taisto Siren and Ari Pdyhiinen for their technical assistance.
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Distribution and abundance of earthworm burrows REFERENCES
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