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The inoculation of Lumbricus terrestris L. in an acidic spruce forest after liming and its influence on soil properties
Soil Bid. Biochem. Vol. 29, No. 314, pp. 611-679, 1997 0 1997 Elsevier Science Ltd. Al1 rights reserved Printed in Grcat Britain PII: !300384717(%)001!&2 0038-0717/97 $17.00 + 0.00
THE INOCULATION OF LUMBRICUS Z-ERRESTRIS L. IN AN ACIDIC SPRUCE FOREST AFTER LIMING AND ITS INFLUENCE ON SOIL PROPERTIES MICHAEL
JUDAS,‘* JÜRGEN
SCHAUERMANN’
and KARL-JOSEF
MEIWES
‘11.Zoologisches Institut der Universität, Abt. Ökologie, Berliner Str. 28, 37073 Göttingen, Germany ‘Niedersächsische Forstliche Versuchsanstalt, Abt. A - Waldwachstum, Grätzelstr. 2, 37079 Göttingen, Germany (Accepted 24 June 1996) Smnmary-At a formerly limed study site in a spruce forest on acidic soil in the Solling mountains, Centra1 Germany, adult or near adult specimens of Lumbricus terresfris were inoculated. The establishment of a reproducing population was monitored for four years. Burrowing activity was detected down to 50 cm, with locally marked incorporation of organic matter to a depth of 20 cm. Chemical changes due to lime particles were restricted to earthworm burrows and a thin surrounding soil layer. A random sample of soil cores revealed no differences in soil chemical characteristics between limed plots with or without L. terrestris. 0 1997 Elsevier Science Ltd
INTRODUaION
In German forests on acid soil superficial liming is widely used as a measure against detrimental effects of acid emissions. The transport of lime down the soil profile is often regarded as insutlicient to work effectively for soil amelioration. Although acid soils in genera1 and spruce forests in particular appear to be unsuitable habitats for Lumbricus terrestris L., it was considered possible to inoculate this deep-burrowing earthworm species at a site that had been limed some years ago and had developed a dense and species-rich ground flora. A successful inoculation of L. terrestris was regarded to possibly enhance the downward movement of lime by their burrowing activity. We addressed the following questions with the experiment:
(1) Does the application of lime in a spruce forest on acid soil create a habitat suitable for the survival of L. terrestris specimens? (2) Does a reproducing earthworm population establish? (3) Is there a change of soil chemical properties attributable to the activity of L. terrestris?
MATERIAL AND METHODS
Study site
The experimental site is situated on the plateau of the Solling mountains in centra1 Germany ca. *Author for correspondence. Fax: + 551 395448. SBB 29/3-4-P
55 km northwest of Göttingen at an altitude of ca. 500 m. It is part of the area that was studied intensively in an IBP project (Ellenberg et al., 1986). Average yearly rainfall and air temperatures are 1045 mm and 6.6”C, respectively. Parent material of soil formation is a 0.2-1 m loess layer on Buntsandstein with soil pH(CaClz) values ranging between 3 and 4. The spruce forest is a TrientalisPiceetum with trees about 110 years of age. The forest is a plantation replacing a former beechwood which would represent the natura1 climax vegetation in the area. The site for the inoculation experiment is part of a 0.1 ha plot which was established in 1975 in order to study the effects of artificial liming (cf. Schauermann, 1987; Matzner, 1985). Lime was applied to the surface in 1975 (4.4 t ha-’ slag lime) and 1980 (4 t ha-’ dolomitic lime). Inoculation and sampling of earthworms
The experiment was an unreplicated inoculation trial using 10,000 earthworms for an area of 400 m*. The earthworms were obtained from a commercial trader which causes uncertainty about their origin and genetic homogeneity. Al1 appeared to be adult or subadult specimens. The inoculation followed a systematic pattern: holes of fingersize spaced at 35 cm intervals on lines 1 m apart were dug into the ground with a fork, and single specimens were placed into each hole. The holes were sealed with wood-pulp so as to prevent the earthworms from immediately leaving the soil and to cause them to start some burrowing activity. The inoculation was carried out in June 1986. Sampling for L. terrestris took place in June 1988, 677
678
Michael
Judas CI ui.
were extracted by 1989 and 1990. The earthworms the application of 0.5% formaldehyde solution to 16 or 10 plots of 0.0625 or 0.1 m* (3 or 5 1 at three charges, respectively). Sampling was restricted at the three dates to sub-plots or a transect of a few square metres so as to minimize disturbance of the study site. Thus, values given for the population of L. terrestris are influenced both by time and location. Local variation has not been analysed any further.
25
N/m’
20 15 10 5 0
In June 1990 one soil profile 2 m long and 1 m deep was dug to assess the effects of earthworm burrowing activities on a micro-scale. Single burrows were prepared, and soil samples were taken from the content at different depths, from the adjacent 2-3 mm burrow wall, and from non-perturbed soil 5-8 cm away from the burrow. If possible. a sample of the organic layer on top of the burrow was also taken. in November 1991 the average soil chemical properties of the limed study site were compared between the inoculated and the noninoculated plot. Twenty soil cores of 8 cm dia and to 50cm depth were taken on either plot at random. Adjacent samples were pooled in groups of 4 resulting in five mixed samples per plot. Nitrogen and carbon contents, pH(NH&I), and NH&Iextractable cation concentrations were determined.
RESULTS
AND DISCUSSION
The earthworm population Two years after the inoculation monitoring of L. terrestris started with different strategies, either taking random samples (1988, 1990) or systematic samples looking for the distribution pattern (1989). Adult L. terrestris were found in varying numbers (Fig. 1) comparable with the numbers found in a Table 1, Chenncal Depth(cm)
1968
1966
Soil chemical properties
pH
properties
Equivalent
designs each June 1988-1990.
mul1 beechwood on limestone near Göttingen (Judas et al., 1989). Specimens appeared to be largely restricted to the original inoculation lines. Cocoons were found, and the numbers of immature specimens indicate that the population reproduced successfully (Fig. 1). Sampling ceased after 1990 but is to be repeated after a long interval. Ejfects on soil morphology and chemistry Lumbricus terrestris specimens constructed burrows down the soil profile that could be excavated to a depth of 50 cm. Burrows were classified as “new” or “old” according to the burrow lumen showing signs of earthworm activity (e.g. open or filled lumen, clear or broken lining; no particular time scale is associated with old or new). Organic material including lime particles was transported into the burrows and affected the immediate surroundings of the burrow (Table 1). Extractable cations were shifted from Al to Ca, and Mg and pH were higher in the wal1 compared with soil only 5 cm apart. This was most evident in the case of a burrow classified as relatively new (Table 1). NO differente between the plots with or without L. term and around earthworm
of NH&I-extractable
burrows
cations
N (% dry wt)
C (% dry wt)
66
1.66 1.10 0.17 0.14
35.2 21.3 3.0 2.8
21 19 18 20
31 56 52 82
1.79 0.85 0.27 0.21 0.12
37.2 18.0 5.2 3.8 1.9
21 21 19 18 lb
74 80 80
0.47 0.13 0.12
10.0 2.4 2.5
21 18 21
Material (pmol, g-‘)
Oh
(%H)
Wal1 Soil
1-11 1-11 1-11
6.6 5.9 4.4 3.9
1400 521 114 110
Oh content Wal1 Soil Soil
0-11 0-11 0-1 1-11
4.3 4.0 4.0 3.1 3.9
516 243 139 139 101
3
Content Wal] Soil
10-20 10-20 10-20
4.0 3.9 3.9
169 101 108
3 3 5
Content
1980
1.
plots and with different
of soil material
fracttons
1989
Abundance of L. terresrris after inoculation in a limed spruce forest. 10,000 specimens were inoculated on 400 m2 in June 1986. Samples were taken at different subFig.
(%Ca) NW burrow 66 65 41 13 Old burrow 74 42 28 28 8 Mixed sample 15 10 8
(%Mg)
34 33 30 IS Ih 12 10
II
6 5
C-to-N rat10
(%Al)
0 0 26
Material, Oh = material above the burrow openings; content, material within the burrow; wall, 2-3 mm of mineral soil adjoining row; soil, mineral soil 5-8 cm distant from the burrow. The mixed sample is of two old burrows which no opening could be prepared pH and cations were determined in NH,CI extracts.
the burat 10-15 and 13-20 cm depth for
Lumbricus terrestris Table 2. Chemical Inoculation
With
Depth(cm)
of random
0-2.5
3.8 0.4 3.7 0.2 3.8 0.2 4.0 0.1 4.2 0.1 4.2 0.1 3.6 0.3 3.6 0.2 3.7 0.1 4.0 0.1 4.1 0.1 4.2 0.1
5-10 10-20 20-30 30-50 0-2.5 2.5-5 5-10 10-20 20-30 30-50
Values given are means and SD derived NH4Cl extracts.
soil cores from sites with or without NH,CI-extractable
PH
2.5-5
Without
orouerties
Ca
Mg
Al
13.5 9.6 10.4 5.7 4.0 2.6 0.08 0.04
56 22 25 9 12 6 6 4 2.3 0.9 1.6 0.2 49 17 21 6 9 2 5 1 2.0 0.8 1.6 0.5
20.7 11.8 ll.9 5.5 1.2 3.5 3.7 2.2 2.1 0.8 1.4 0.3 17.5 8.1 9.8 4.4 5.5 2.1 3.5 1.6 1.7 0.8 1.5 0.6
75 24 87 10 89 8 70 9 56 6 52 5 79 16 88 8 90 6 67 8 54 8 49 6
0” B 18.2 1.2 10.8 4.1 3.4 1.2 0 0 0 0 0 0
from 20 samples that were pooled
burrows or their diluted by mixing
CONCLUSION
We conclude that the results of this experiment indicate that L. terrestris may be suited for inoculation in previously uninhabited biotopes if supported by the creation of sufficient living conditions. Indeed a viable and reproducing population of L. terrestris was established. But burrows incorporated
organic
material
and
in groups
lime par-
L. terrestris N (% dry wt)
C (% dry wt)
0.43 0.02 0.27 0.03 0.19 0.01 0.13 0.01 0.10 0.01 0.08 0.01 0.37 0.08 0.21 0.0 1 0.16 0.01 0.11 0.01 0.08 0.01 0.07 0.01
7.8 0.5 4.4 0.6 3.0 0.3 1.9 0.3 1.04 0.17 0.67 0.16 7.4 1.9 3.8 0.2 2.7 0.3 1.6 0.2 0.95 0.19 0.62 0.08
of 4 (n = 5). pH and cations
were determined
in
ticles were constructed only locally. A quantitative effect on the soil system seems not to be expected within a few years. Potential long-term effects have yet to be determined.
chemical samples.
Horizontal bioturbation can be accomplished by endogeic species in other habitats, but in the studied spruce forest they were lacking.
with
inoculated
cations (pmol g’)
H
restris could be found from the random soil cores (Table 2). This was to be expected from the restriction of earthworm activity to the inoculation sites and from the absente of the effect of bioturbation away from the burrows. The random soil samples
missed L. terrestris characteristics were
619
inoculation
REFERENCES
Ellenberg
H., Mayer
R. and Schauennann
Okosystemforschung - Ergebnisse 1966-1986. Ulmer, Stuttgart.
J. (1986)
des Sollingprojektes
Judas M., Poser K., Joger H. G. and Schaefer M. (1989) Langfristige Populationsdynamik der Regenwtirmer (Lumbricidae) eines Kalkbuchenwaldes. Verhandlungen der Gesellschaft jììr Ökologie 17, 245-250. Matzner E. (1985) Auswirkungen von Düngung und Kalkune auf den Elementumsatz und die Elemen~erteilung von zwei Waldökosystemen im Solling. Allgemeine Forst-Zeitschrift 41, 1143.-1147. Schauermann J. (1987) Tiergesellschaften der Wälder im Solling unter dem EinfluB von Luftschadstoffen und ktinstlichem Säure- und Düngereintrag. Verhundlungen der Gesellschaft für Okologie 16, 53-62.
THE INOCULATION OF LUMBRICUS Z-ERRESTRIS L. IN AN ACIDIC SPRUCE FOREST AFTER LIMING AND ITS INFLUENCE ON SOIL PROPERTIES MICHAEL
JUDAS,‘* JÜRGEN
SCHAUERMANN’
and KARL-JOSEF
MEIWES
‘11.Zoologisches Institut der Universität, Abt. Ökologie, Berliner Str. 28, 37073 Göttingen, Germany ‘Niedersächsische Forstliche Versuchsanstalt, Abt. A - Waldwachstum, Grätzelstr. 2, 37079 Göttingen, Germany (Accepted 24 June 1996) Smnmary-At a formerly limed study site in a spruce forest on acidic soil in the Solling mountains, Centra1 Germany, adult or near adult specimens of Lumbricus terresfris were inoculated. The establishment of a reproducing population was monitored for four years. Burrowing activity was detected down to 50 cm, with locally marked incorporation of organic matter to a depth of 20 cm. Chemical changes due to lime particles were restricted to earthworm burrows and a thin surrounding soil layer. A random sample of soil cores revealed no differences in soil chemical characteristics between limed plots with or without L. terrestris. 0 1997 Elsevier Science Ltd
INTRODUaION
In German forests on acid soil superficial liming is widely used as a measure against detrimental effects of acid emissions. The transport of lime down the soil profile is often regarded as insutlicient to work effectively for soil amelioration. Although acid soils in genera1 and spruce forests in particular appear to be unsuitable habitats for Lumbricus terrestris L., it was considered possible to inoculate this deep-burrowing earthworm species at a site that had been limed some years ago and had developed a dense and species-rich ground flora. A successful inoculation of L. terrestris was regarded to possibly enhance the downward movement of lime by their burrowing activity. We addressed the following questions with the experiment:
(1) Does the application of lime in a spruce forest on acid soil create a habitat suitable for the survival of L. terrestris specimens? (2) Does a reproducing earthworm population establish? (3) Is there a change of soil chemical properties attributable to the activity of L. terrestris?
MATERIAL AND METHODS
Study site
The experimental site is situated on the plateau of the Solling mountains in centra1 Germany ca. *Author for correspondence. Fax: + 551 395448. SBB 29/3-4-P
55 km northwest of Göttingen at an altitude of ca. 500 m. It is part of the area that was studied intensively in an IBP project (Ellenberg et al., 1986). Average yearly rainfall and air temperatures are 1045 mm and 6.6”C, respectively. Parent material of soil formation is a 0.2-1 m loess layer on Buntsandstein with soil pH(CaClz) values ranging between 3 and 4. The spruce forest is a TrientalisPiceetum with trees about 110 years of age. The forest is a plantation replacing a former beechwood which would represent the natura1 climax vegetation in the area. The site for the inoculation experiment is part of a 0.1 ha plot which was established in 1975 in order to study the effects of artificial liming (cf. Schauermann, 1987; Matzner, 1985). Lime was applied to the surface in 1975 (4.4 t ha-’ slag lime) and 1980 (4 t ha-’ dolomitic lime). Inoculation and sampling of earthworms
The experiment was an unreplicated inoculation trial using 10,000 earthworms for an area of 400 m*. The earthworms were obtained from a commercial trader which causes uncertainty about their origin and genetic homogeneity. Al1 appeared to be adult or subadult specimens. The inoculation followed a systematic pattern: holes of fingersize spaced at 35 cm intervals on lines 1 m apart were dug into the ground with a fork, and single specimens were placed into each hole. The holes were sealed with wood-pulp so as to prevent the earthworms from immediately leaving the soil and to cause them to start some burrowing activity. The inoculation was carried out in June 1986. Sampling for L. terrestris took place in June 1988, 677
678
Michael
Judas CI ui.
were extracted by 1989 and 1990. The earthworms the application of 0.5% formaldehyde solution to 16 or 10 plots of 0.0625 or 0.1 m* (3 or 5 1 at three charges, respectively). Sampling was restricted at the three dates to sub-plots or a transect of a few square metres so as to minimize disturbance of the study site. Thus, values given for the population of L. terrestris are influenced both by time and location. Local variation has not been analysed any further.
25
N/m’
20 15 10 5 0
In June 1990 one soil profile 2 m long and 1 m deep was dug to assess the effects of earthworm burrowing activities on a micro-scale. Single burrows were prepared, and soil samples were taken from the content at different depths, from the adjacent 2-3 mm burrow wall, and from non-perturbed soil 5-8 cm away from the burrow. If possible. a sample of the organic layer on top of the burrow was also taken. in November 1991 the average soil chemical properties of the limed study site were compared between the inoculated and the noninoculated plot. Twenty soil cores of 8 cm dia and to 50cm depth were taken on either plot at random. Adjacent samples were pooled in groups of 4 resulting in five mixed samples per plot. Nitrogen and carbon contents, pH(NH&I), and NH&Iextractable cation concentrations were determined.
RESULTS
AND DISCUSSION
The earthworm population Two years after the inoculation monitoring of L. terrestris started with different strategies, either taking random samples (1988, 1990) or systematic samples looking for the distribution pattern (1989). Adult L. terrestris were found in varying numbers (Fig. 1) comparable with the numbers found in a Table 1, Chenncal Depth(cm)
1968
1966
Soil chemical properties
pH
properties
Equivalent
designs each June 1988-1990.
mul1 beechwood on limestone near Göttingen (Judas et al., 1989). Specimens appeared to be largely restricted to the original inoculation lines. Cocoons were found, and the numbers of immature specimens indicate that the population reproduced successfully (Fig. 1). Sampling ceased after 1990 but is to be repeated after a long interval. Ejfects on soil morphology and chemistry Lumbricus terrestris specimens constructed burrows down the soil profile that could be excavated to a depth of 50 cm. Burrows were classified as “new” or “old” according to the burrow lumen showing signs of earthworm activity (e.g. open or filled lumen, clear or broken lining; no particular time scale is associated with old or new). Organic material including lime particles was transported into the burrows and affected the immediate surroundings of the burrow (Table 1). Extractable cations were shifted from Al to Ca, and Mg and pH were higher in the wal1 compared with soil only 5 cm apart. This was most evident in the case of a burrow classified as relatively new (Table 1). NO differente between the plots with or without L. term and around earthworm
of NH&I-extractable
burrows
cations
N (% dry wt)
C (% dry wt)
66
1.66 1.10 0.17 0.14
35.2 21.3 3.0 2.8
21 19 18 20
31 56 52 82
1.79 0.85 0.27 0.21 0.12
37.2 18.0 5.2 3.8 1.9
21 21 19 18 lb
74 80 80
0.47 0.13 0.12
10.0 2.4 2.5
21 18 21
Material (pmol, g-‘)
Oh
(%H)
Wal1 Soil
1-11 1-11 1-11
6.6 5.9 4.4 3.9
1400 521 114 110
Oh content Wal1 Soil Soil
0-11 0-11 0-1 1-11
4.3 4.0 4.0 3.1 3.9
516 243 139 139 101
3
Content Wal] Soil
10-20 10-20 10-20
4.0 3.9 3.9
169 101 108
3 3 5
Content
1980
1.
plots and with different
of soil material
fracttons
1989
Abundance of L. terresrris after inoculation in a limed spruce forest. 10,000 specimens were inoculated on 400 m2 in June 1986. Samples were taken at different subFig.
(%Ca) NW burrow 66 65 41 13 Old burrow 74 42 28 28 8 Mixed sample 15 10 8
(%Mg)
34 33 30 IS Ih 12 10
II
6 5
C-to-N rat10
(%Al)
0 0 26
Material, Oh = material above the burrow openings; content, material within the burrow; wall, 2-3 mm of mineral soil adjoining row; soil, mineral soil 5-8 cm distant from the burrow. The mixed sample is of two old burrows which no opening could be prepared pH and cations were determined in NH,CI extracts.
the burat 10-15 and 13-20 cm depth for
Lumbricus terrestris Table 2. Chemical Inoculation
With
Depth(cm)
of random
0-2.5
3.8 0.4 3.7 0.2 3.8 0.2 4.0 0.1 4.2 0.1 4.2 0.1 3.6 0.3 3.6 0.2 3.7 0.1 4.0 0.1 4.1 0.1 4.2 0.1
5-10 10-20 20-30 30-50 0-2.5 2.5-5 5-10 10-20 20-30 30-50
Values given are means and SD derived NH4Cl extracts.
soil cores from sites with or without NH,CI-extractable
PH
2.5-5
Without
orouerties
Ca
Mg
Al
13.5 9.6 10.4 5.7 4.0 2.6 0.08 0.04
56 22 25 9 12 6 6 4 2.3 0.9 1.6 0.2 49 17 21 6 9 2 5 1 2.0 0.8 1.6 0.5
20.7 11.8 ll.9 5.5 1.2 3.5 3.7 2.2 2.1 0.8 1.4 0.3 17.5 8.1 9.8 4.4 5.5 2.1 3.5 1.6 1.7 0.8 1.5 0.6
75 24 87 10 89 8 70 9 56 6 52 5 79 16 88 8 90 6 67 8 54 8 49 6
0” B 18.2 1.2 10.8 4.1 3.4 1.2 0 0 0 0 0 0
from 20 samples that were pooled
burrows or their diluted by mixing
CONCLUSION
We conclude that the results of this experiment indicate that L. terrestris may be suited for inoculation in previously uninhabited biotopes if supported by the creation of sufficient living conditions. Indeed a viable and reproducing population of L. terrestris was established. But burrows incorporated
organic
material
and
in groups
lime par-
L. terrestris N (% dry wt)
C (% dry wt)
0.43 0.02 0.27 0.03 0.19 0.01 0.13 0.01 0.10 0.01 0.08 0.01 0.37 0.08 0.21 0.0 1 0.16 0.01 0.11 0.01 0.08 0.01 0.07 0.01
7.8 0.5 4.4 0.6 3.0 0.3 1.9 0.3 1.04 0.17 0.67 0.16 7.4 1.9 3.8 0.2 2.7 0.3 1.6 0.2 0.95 0.19 0.62 0.08
of 4 (n = 5). pH and cations
were determined
in
ticles were constructed only locally. A quantitative effect on the soil system seems not to be expected within a few years. Potential long-term effects have yet to be determined.
chemical samples.
Horizontal bioturbation can be accomplished by endogeic species in other habitats, but in the studied spruce forest they were lacking.
with
inoculated
cations (pmol g’)
H
restris could be found from the random soil cores (Table 2). This was to be expected from the restriction of earthworm activity to the inoculation sites and from the absente of the effect of bioturbation away from the burrows. The random soil samples
missed L. terrestris characteristics were
619
inoculation
REFERENCES
Ellenberg
H., Mayer
R. and Schauennann
Okosystemforschung - Ergebnisse 1966-1986. Ulmer, Stuttgart.
J. (1986)
des Sollingprojektes
Judas M., Poser K., Joger H. G. and Schaefer M. (1989) Langfristige Populationsdynamik der Regenwtirmer (Lumbricidae) eines Kalkbuchenwaldes. Verhandlungen der Gesellschaft jììr Ökologie 17, 245-250. Matzner E. (1985) Auswirkungen von Düngung und Kalkune auf den Elementumsatz und die Elemen~erteilung von zwei Waldökosystemen im Solling. Allgemeine Forst-Zeitschrift 41, 1143.-1147. Schauermann J. (1987) Tiergesellschaften der Wälder im Solling unter dem EinfluB von Luftschadstoffen und ktinstlichem Säure- und Düngereintrag. Verhundlungen der Gesellschaft für Okologie 16, 53-62.