Microbial carbon turnover in beech forest soils worked by Aporrectodea caliginosa (Savigny) (Oligochaeta:Lumbricidae)

0038-0717/92 S5.00+ 0.00

Soil Biol. Biocfrent.Vol. 24, No. 2, pp. 171-177,1992 Print& in Great Britain. All rights reserved

Copyright 0 1992Pcrgamon Pmas plc

MICROBIAL CARBON TURNOVER IN BEECH FOREST SOILS WORKED BY APORRECTODEA CALIGINOSA (SAVIGNY) (OLIGOCHAETA :LUMBRICIDAE) V. Wo~mts’*

and R. G. JOERGENSEN*

‘Abt~lung Oekologie, II. Zoologisches Institut, Berliner Strasse 28, D-3400 Goettingen and *Institut fuer Bodenwissenschaften, Geor~August-Universitaet, von-Siebold-St&e 4, D-3400 Goettingen, Fed. Rep. Germany (Accepted 25 August 1991) Summary-Effects of the endogeic earthworm species Aporrectodea calighsa (Savigny) on the edaphic microflora were studied in six German beech forest soils using the f~ga~on~x~action method. The following response variables were measured: biomass (C&, C incorporation from r4C-labelled beech leaf litter (‘“C,,& and two metabolic quotients (qC02: pg CO& fig-’ G, h-r; qr4C0,: p “CO& pg-’ 14Ctich-l). After removing the earthworms from the experimental containers at day 21, the experiment ran for a further 21 days to study the long-term alteration of microbial performance in earthworm worked soils. At day 21, C,, and 14Cti were reduced in the earthworm treatments of five soils and qC0, and q’4C02 were increased in all soils. Effects on CA and ‘*C,, were not correlated to each other. The day 21 effects of A. caZig~~~aon C,, and qC0, declined, while the stimulation of qt4C02 increased with increasing soil acidity. Day 42 m~u~ments showed that the long-term effects of A. caliginosa on microbial C use were highly soil specific and were opposite to the effects measured at day 21 in most of the soils. It is concluded from these results that A. caliginma alters the biomass and the metabolic activity of the edaphic microflora over a wide range of soils, that these alterations are highly soil and resource specific and that the microbial C turnover in soils freshly worked by A. caliginosa is significantly different from the microbial C turnover in aged casts and burrows.

INTRODUCTION

This is the second part of a study on the relationship between microbial C turnover and environmental factors in beech forest soils sampled in the Goettinger Wald area (Germany). In the first part of the study, we analysed the relations~p between soil conditions and microbial performance (Walters and Joergensen, 1991). It was shown that differences in the C content of soils could partly be explained by the effect of soil acidification on the carbon use of microorganisms. This part of the study focuses on an environmental factor which is most irn~~nt for the edaphic microflora in the area where the soils were collectedthe burrowing activity of endogeic earthworms (Schaefer, 1990). We chose Aporrectodea caliginosa (Savigny) as an example of endogeic earthworms because this species dominates the biomass of this geophagus earthworm group in the Goettinger Wald area (Judas, 1989). “Earthworms, which.. . aerate the medium with burrows, mix organic and inorganic, living and nonliving elements indiscriminately and smear their milieu with mucus, urine and faeces are distressing subjects for microbiology” (Satchell, 1983). The microflora in guts, casts and burrows of earthworms has nevertheless been intensely studied (Edwards and Lofty, 1977; Satchell, 1983; Lee, 1985). One serious problem in earthworm microbiology is, however, that

it is impossible to relate the results of descriptive studies on the composition of the gut microflora or on the microbial succession in casts to the results of investigations on C and N mineralization in earthworm worked soils. We tried to overcome this shortcoming, at least in part, by applying the recently developed fumigation extraction technique for microbial biomass estimation (Vance et al., 1987) to quantify the effects of A. caliginosa on microbial performance in soil. This method can be used to obtain information about both the performance of the edaphic microflora and the quantitative contribution of the microflora to nutrient turnover in soil (Jenkinson, 1988). By using a similar approach we have shown in previous studies that elaterid larvae and springtails strongly affect the biomass and the metabolic activity of the soil microflora (Walters, 1989, 1991). In the present study, we address the following questions: Are A. cafiginosa effects on microbial C turnover affected by soil conditions? Does A. cafiginosa alter the use of different C sources by the edaphic microflora in a different and possibly soil-specific way7 MATERIALS AND MRTHODS Soils The

*Author for correspondence.

situated 171

area in which the soils were collected is in the Goettinger Wald (Lower Saxony,

V. WOLTERSand

i72

R. G. JOWOENSBN

Germany) on a plateau 400-420m above sea level, covered by lOO-130yr-old beech trees (Fagu.r syfuuficu L.) (Walters, 1983). Mean annual temperature is 7.9”C and mean annual p~ipi~tion 720 mm. The bedrock is shell-lime. Three soils (O-10 cm) were collected from the Treppenweg area and three soils from the Klein Lengden area in May 1989. According to the German classification system (AK Rodensystematik, 1985). the soils of the Treppenweg area are classified as follows: Rendxina [Orthic Rend&a (FAO), Typic Rendoll (USDA)], Terra fusca Rendxina [Chrome-Calcic Cambisol (FAO), Lithic Rendoli (USDA)] and Terra fusca [Chromic Cambisol (FAO), Typic Eutrochrept (USDA)]. The soils of the Klein Lengden area are again a Rend&a and two Acid Brown Earths [Dystric Cambisol (FAO), Typic Dystrochrept (USDA)]. The Rend&a sampled in the Treppenweg area is referred to as Rend&a II later in the text, the one sampled in the Klein Lengden area as Rendxina I. A more detailed description of the soils is given in Wolters and Joergensen (1991). Important soil factors are summarized in Table l(a).

The structural components of “C-1abelled leaf litter (68 mg: roughly corresponding to an amount of 70g rnv2 or 25% of annual C input via leaf-litter) were added to each flask at the beginning of the experiment to study the mineralization of undecomposed beech litter. The specific activity of the litter was 1 Rq pg-’ C. Labelling and extraction of soluble carbohydrates were described by Walters (1989). The flasks were stoppered with a rubber bung and kept at 10°C under permanent darkness. They were opened daily for approx. 20 min to allow gas exchange. Evolved CO,-C and “CO2-C was absorbed in 1 M NaOH. Correction for earthworm respiration was not made because its contribution to CO, and “CO1 evolution was assumed to be negligible. Earthworms removed at day 21 were kept for 12 h on moist filter paper to allow gut clearance before weighing. The farces released during this period were dried and weighed. An aliquot of the faeces was inspected microscopically before drying.

Experimental design and setting The experiment was completely 3-way factorial, with 6 soil treatments x 2 earthworm treatments x 2 time treatments. Each soil x earthworm combination was set up with 5 replicates. After sieving (< 2 mm), moist soil corresponding to 70 g dry weight was placed into 1 I Erlenmeyer flasks. Sub-adult A. caliginosa were collected in the Goettinger Waid area 2 weeks before the experiment began. The fresh weight of each worm was 375 mg (f 10%) (the fresh weight of adult A. c~ig~su in the Goettinger Wald area is in the range of 450-500mg). We did not investigate the structure of the earthworm population in the areas where the soils had been collected. However, individuals of A. culiginosa were randomly found in all six soils during sampling of the substrata. Five days before the experiment began, each worm was placed separately into substratum of the respective soil treatment, in order to avoid input of extra nutrients or microflora from other soils. At day 1, one A. caiiginosa was added to each of half of the experimental containers. At day 21, all A. cdiginosa were carefully removed and the experiment ran for a further 21 days without active earthworms. Tabk la. Soil Abbreviationa used in figures

Terra fuaaa

hdzinat Terra fuacnt Acid Brown E?artb I* Acid Brown Earth II* Pooled Cv$ f%

lKkin Len*;

C, (mgg-’

soi:

Analytical procedures CO,-C evolved during incubation was calculated by titration. “‘CO2-C production was calculated from 0.5 ml aliquots by scintillation counting. At days 21 and 42, soil corresponding to 20g dry weight was sampled from each flask for biomass determination. Soil microbial biomass (C&) was measured by the fumigation extraction method (Vance et al,, 1987). Organic C extracted from 10 g fumigated and 10 g non-fumigated soil of each experimental container with 40ml 0.5 m K2SO4 was measured using a Dohrman DC 80 automatic analyser. Soil microbial biomass C was calculated using the formula [(C extractable from fumigated soils) - (C extractable from non-fasts soils)] x 2.22 (Wu et al., 1990). “‘C-content of the microbial biomass (“Cd) was determined in portions of the K2SO4 extracts by scintillation counting. The metabolic quotients qC02 and q”C02 @g CO,-C pg-’ C& h-‘; cf. Pitt, 1975) were calculated from the COTC and “CO2-C evolved during the last 3 days before Cd and “Cd determination. Analysis of soils was carried out using standard methods; for details see Wolters and Joergensen (1991). The signiticance of treatment effects was tested by means of a 3-way ANOVA. Figures presented here are arithmetic means, with signilicance tests based upon app~p~~ly transformed data. Differences between means were tested propertics c_/N,

pH-H,O

ca,

CEC

(req s-’ win

CkY % mineral soil

RI RI1

96.6 83.3

7.37 6.40

13.1 13.0

7.5 8.3

348 347

359

35 47

TFR

64.0

5.14

12.5

8.2

309

g

47

IF AM ABII

44.8 31.3 31.7 0.5

3.14 2.28 2.14 0.61

12.0 13.6 14.8 0.5

3.8 4.8 5.0 2.0

IS7 40 33 2.4

194 90 63 3.3

45 25 14 8.4

yhppcnwrg;

ghcffent

of vari8tion.

Microbial carbon turnover in A. cufigaroru worked soils Tabk l(b). Soil microbial biomass (C,

and I’&)

and metabolic mcilicients

C,’ RcndziM I RcndziM II Terra fusca RendziM Terra fwca Acid Brown Eartb I Acid Brown Earth II Pooled CV f %

173

(qCOrand q’%!Q) in the aotrou 41day 21 ti

‘cd*

day 42

S’QM

PCW

DaY 21

Dav 42

Day 21

Day 42

my 21

Day 42

&y ?I

I)ry 42

1520 1198 1170 819 a39 703 12

1722 I382 1138 769 501 607 16

2.59 3.02 1.65 1.11 1.26 1.01 20

2.03 2.26 1.58 1.09 1.02 1.17 I3

1.45 1.69 1.63 2.42 2.15 2.43 -

I .22 1.55 I.75 3.26 4.54 8.63 -

3.50 2.96 3.24 3.70 2.98 2.30 -

3.83 2.49 2.22 3.17 3.77 2.94 -

lpg g-l soilytmg CO& h-l g-’ C,*; $mg “CO&h-

g-’ “C,,,*

using the Tukey test. The effect of A. caliginosa on the response variables was calculated by subtracting the values measured in the controls from those measured in the respective A. caliginosu treatments. Results of the control treatments are listed in Table l(b) for easy comparison (cf. Wolters and Joergensen, 1991). Linear correlation between earthworm effects and variables for soil conditions was calculated using standard methods. REBULTS

Earthworm activity

Daily inspection of the experimental containers showed that A. caliginosa was actively burrowing in every soil. This was also shown by the enormous cast production as well as by the complete mixing of labelled beech leaf litter with mineral soil. Soil conditions did not seem to affect the activity and feeding behaviour of the worms. This is concluded from the fact that the amount of faeces deposited by A. caliginosa during the 12 h incubation after removal from the experimental containers at day 21 was not significantly different between soils. Microscopical observation of the faeces indicated geophagous behaviour in every soil. General effects of treatments The results of the 3-way ANOVAs are listed in Table 2. Significant main effects of soil reflect the decrease in Cd and “C,ic as well as the increase in metabolic activity with increasing soil acidity (Table 1). Significant main effects of time and soil x time interactions indicate alterations in the metabolic quotients and C& during incubation. These results were discussed in detail by Wolters and Joergensen (1991) and will not be repeated here. Main effects of A. caliginosa were significant for Cd and q”COr (Table 2) retlecting a consistent alteration of these response variables in the earthworm treatments. Significant A. caliginosa x soil interactions indicate that the effect of both A. caliginosu and soil on C, and qC0, were strongly affected by each other. Significant A. caliginosa x time interactions reflect a strong alteration of C&, i’Cti and q”COr in the earthworm treatments 3 weeks after A. caliginosa had been removed from the experimental containers. No significant second-order interactions were detected.

Soil microbial biomass C, was significantly reduced in the A. caliginosa treatments of all soils at day 21, except those of Acid

Brown Earth II (Fig. la). Negative correlations to pH, Ca, and CEC indicate that the extent of biomass depression in the earthworm worked soils declined with increasing soil acidity (Table 3). Negative correlation to C,, and N, indicate that the effect of A. caliginosa on qC0, was significantly affected by soil organic matter. At day 42, the differences between C, in soils worked by A. caliginosa and C,, in the respective controls was similar to the differences measured at day 21 in only two soils (Acid Brown Earth II, Terra fusca Rendxina; Fig. la). In

Tabk 2. Red&s of the three-way ANOVAs DF (a) Microbial biomass (IcgC, g-’ roil) 1 A. caliginaco (A) 5 Soil (S) I Time (T) 5 AXS 1 AxT 5 SXT 5 AxSxT 72 Error

SS%

1.1 3.3 1.6 6.9 19.8

(b) Microbial “C incorp. (pg”C& g-’ soil) A. caliginasa (A) : 47.2 Soil (S) I Time (T) 5 AxS I Y2 AxT SxT : AxSxT 72 42.7 Error (c) Metaboliffiquotientqco, A. caliginosa (A) Soil (S) Tiie (T) AxS AxT SxT AxSxT Error

Ft 3.41. 46&v*** 3.96. 2.40’ 5.97.’ 4.9s*** NS

15.K* NS NS 5.33. ::

(r&or-c g-1 c, Ii-‘) 1 5 1 5 1

15.5 2.7 11.2 -

: 72

z 56.6

(d) Metabolii quotient q”C0, @<‘CO& &’ ‘c, A. caliginara (A) 5 : Soil (S) II 9 Time 0 : L AxS I 11.2 AxT 5 SxT 5 AxSxT 72 58.3 Error

NS NS NS h-l) 10.86** NS 14.74.”

t****p < 0.0001; ?**P < 0.001; l*p < 0.01; lP < 0.05. NS not signillcanl.

NS NS

V. WOLTERS and R. G. J~~~GENSEN

174

q day ABI

21

AElI

l-F

soils

TFR

RI

RII

Fig. 1. Effect of the endogeic earthworm species A. culiginosa on two different C pools of the microflora in six different beech forest soils. Triangles indicate significant differences between earthworm treatments and respective controls (P < 0.05). (See Table 1 for explanation of soil abbreviations.) a-Microbial biomass (C&); b-C incorporated from structural components of “C-1abelled beech leaf litter (“C,,&.

the remaining soils, the A. culiginosa effect was either inverted (Acid Brown Earth I, Rendzina II) or was no longer significant (Rend&a I, Terra fusca). The difference between earthworm treatments and mspective controls at day 42 was not linearly correlated to any of the variables for soil conditions measured (Table 3). Metabolic quotient qC0, The qC0, was increased in the A. culiginosu treatments of every soil at day 21. Differences between means were not significant. Linear correlation to pH, Ca, and CEC, justified by the significant interactions with soil revealed by the ANOVA (Table 2), indicate that the stimulation of qCO* in the earthworm worked soils declined with increasing soil acidity (Table 3). In addition, the effect of A. culiginosu on qC0, was signiticantly a&ted by clay content.

Significant differences between means in three of the soils at day 42 indicate that the long-term effect of A. culiginosu on qC0, was stronger than the short-term effect in half of the soils (Fig. 2a). In contrast to the general stimulation of qC0, at day 21, qC0, was reduced in the A. coliginosu treatments of all soils except those of the Terra fusca Rendxina at day 42 (Fig. 2a). This effect was not linearly correlated to any of the variables for soil conditions measured (Table 3). Microbial use of “4C-kabelled leaf litter 14C,, was significantly increased in the earthworm treatments of Acid Brown Earth I at day 21 and significantly reduced in those of the remaining soils (Fig. lb). The effect of actively burrowing A. culiginosu on i4Cti was thus very similar to the effect on Cti (Fig. la). However both effects were not

Microbial carbon hunover in A. cdiginosa worked soils Table 3. Comlation

175

matrix of soil propcrtics and A. culiginosa effectst on microbial biomacw and metabolic quotients at day 21 and day 42 A’% mk

AC, Day 21

4COz

Day 42

Day 21

Day 42 0.64 0.59 0.07

C, N, C,N

-0.92’. -0.93’. 0.48

-0.27 -0.33 0.52

-0.50 -0.49 0.03

& C&X (Jay

-0.94.’ -0.96.; -0.96’. -0.70

-0.62 -0.49 -0.50 -0.57

-0.60 -0.51 -0.54 -0.33

0.24 0.42 0.41 -0.02

dq”W

Day 21

Day 42

Day 21

Day 42

0.69 0.73 -0.65

0.53 0.56 -0.43

- 0.w - 0.87. 0.62

-0.63 -0.55 -0.46

0.72 0.64 0.67 0.57

-0.81. -0.90* -0.88. -0.75

-0.41 -0.37 -0.43 0.19

0.9419 0.88. 0.87. 0.89’

tDiffercnce between the treatments with A. ca/iginosa minus the respective control. AC,: cfTcct on microbiil biomass; A”t&: microbial C incorporation from “C-lab&d beech leaf litter; AqCOz and Aq”C0,: cffccts on metabolic quotients. lP < 0.05; l*p < 0.01.

linearly correlated to each other, indicating resource specificity in the effect of A. caliginosa on microbial C use. i4Ctic was still significantly increased in the Acid Brown Earth I at day 42. At this time, i4Ctic was also increased in the earthworm treatments of both

Rend&as and was not significantly different from the respective controls in the remaining soils. Neither at day 21 nor at day 42 was the effect on 14Cticlinearly correlated to any of the soil factors measured (Table 3).

Fig. 2. E&t of the endogeic earthworm species A. caligino~a on two diRerentmetabolic quotients of the microflora in six different beech forest soils. Triangles indicate @Scant differences between earthworm treatments and respective controls (P < 0.05). (See Table 1 for explanation of soil abbreviations.) a: qC0, @g CO& peg-’ C,, h-l); b: q” CO2 @g “CO& pg-’ “C& h-l).

SBB 242-G

effect on

V. WOLTERSand

176

The q’4C02 was significantly increased in the earthworm treatments of all soils at day 21 (Fig. 2b). Opposite to qC02, the stimulation of qi4C02 was negatively correlated to pH, Ca,, and CEC (Table 3). Negative correlations to C,,, and N1 indicate that the effect of A. caliginosu on the use of C from freshly fallen beech leaf litter for metabolic demands declined with increasing amounts of soil organic matter. Three weeks after the earthworms had been removed, sig niflcant effects of A. cu~jgjnosa on qi4C0, were confined to the Terra fusca and Rendzina II (Fig. 2b). As for all other response variables, A. caliginosa effects on q14C02 were not linearly correlated to any of the soil factors measured at day 42 (Table 3). DISCUSSON

We measured the size of the microbial biomass, the microbial incorporation of 14C and the metabolic quotients qC02 and qi4C02 to study microbial performance in six different beech forest soils worked by the endogeic earthworm species A. cuiiginosu. The results show that the fumigation~xtraction method is well suited for studying the effect of earthworms on microbial biomass in soil. The applicability of the fumigation-extraction method over the whole range of soil pHs (Vance et al., 1987) made it possible to overcome some of the shortcomings of the fumigation-incubation method applied in previous studies (Walters, 1989, 1991). Another advantage of the fumigation-extraction method in the context of soil zoological research is that it is not necessary to incubate soils at elevated temperatures. The following general conclusions can be drawn from the results: (1) A. culiginosu si~ifi~antly alters the biomass and the metabolic activity of the edaphic microflora over a wide range of soils. (2) The effect of A. culiginosa on the edaphic microflora is highly soil and resource specific. (3) The microbial C turnover in soils freshly worked by A. caliginosu is significantly different from the microbial C turnover in aged casts and burrows. A dependency of earthworm effects on soil conditions has been demonstrated for plant growth (Atlanvinyte et al., 1968), soil pH (Salisbury, 192.5), aggregate stabilization (Marinissen and Dexter, 1990) and microbial activity (Shaw and Pawiuk, 1986). The close correlations between soil conditions and earthworm effects demonstrated in our study thus concur with the results of other authors. By using soils at different states of acidification we have shown that only the short-term effects of A. caliginosu measured at day 21 were linearly correlated to variables for soil conditions. This indicates that only the early stage of microbial succession in earthworm worked soils is immediately affected by factors such as nutrient availability. The lack of correlations in aged casts and burrows reflects that later stages of microbial succession are more exposed to a complex pattern of

R. G. JOERGENSEN environmental factors, including biotic interactions. Similar conclusions have been drawn from investigations on the microbial colonization of different organic substrata (Swift, 1984, Heal and Dig&on, 1985). Our measurements offer the possibility of finding a quantitative basis for microbial succession in earthworm casts. This will be outlined in the following comparison between our results and results published in the literature. The growth of bacteria and actinomycetes is strongly favoured in freshly deposited earthworm casts (Ponomereva, 1953; Kozlovskaya and Zhdannikova, 1966) and the initial phase of microbial succession in casts is accompanied by an intense mineralization of organic compounds (Nowak, 1975). Soil bacteria which colonize freshly de~sited substrata generally fix a smaller mount of carbon in their cells and have a higher turnover rate than fungi, which dominate the microbial biomass in undisturbed soils (Paul and Clark, 1989). This may explain the biomass depression as well as the increased metabolic quotients observed in the A. culigjnosu trea~ents of five soils at day 21. During the ageing of casts, the growth of fungi sets in, the metabolic activity gradually declines and N is immobilized (Parle, 1963). The increased microbial biomass and the comparatively low metabolic quotient in many of our soils at day 42, i.e. 3 weeks after A. diginosu had been removed, closely parallel these findings. It should be noted, however, that we essentially measured a mixture of A. culiginosu effects, i.e. even for the day 21 measurements we did not differentiate between fresh and old casts or between casts and burrows. This may explain some of the apparent inconsistencies in our data. For example, the increased biomass in the earthworm treatments of Acid Brown Earth II at day 21 may indicate that the effect of A. caliginosu on the microflora in this soil was completely different from the effect on the microflora in the other soils. Alternatively, it may simply indicate that the microbial succession in this soil took place at such a fast rate that the biomass increase in the aged casts, which were accumulating over the first 21 days of the experiment, rapidly outweighed the biomass depression in fresh casts. Biomass determinations have to be carried out more frequently to test this hypothesis. Investigations of soils to which earthworms had been newIy introduced show that “during the transitional phase (of the ecosystem), earthworms may act as driving variables determining both the rate of change and the new equilibrium state” (Anderson, 1988). As far as we know, however, no one has tried to relate the effect of earthworms (or that of any other soil invertebrates) to a pedogenetic sequence of soils. Pedogenesis is normally accompanied by soil acidification in Central Europe (Ulrich, 1987). The use of soils at different stages of acidification in our study shows that the effect of A. caliginosu on microbial C use may strongly change during pedogenesis.

Microbial carbon turnover in A. caliginosa worked soils

Both the depression of Ctic and the stimulation of qCOZ in the earthworm treatments at day 21 declined with increasing soil acidity, reflecting that the effect of A. caliginosa on the soil microflora may lose its significance in acidified soils. The increased stimulation of qi4C02 in the acid soils indicates that endogenic earthworms may even accelerate C loss from these soils by favoring the inefficient use of C from freshly fallen litter for metabolic demands (cf. Wolters and Joergensen, 1991). The strong mixture of undecomposed beech leaf litter and mineral soil in all A. caliginosa treatments as well as the fact that the incorporation of litter into the microbial biomass was not affected by factors indicating soil acidification, undoubtedly counteracts this process. One of the most important effects of endogeic earthworms in the Goettinger Wald area is the stimulation of N mineralization (Scheu, 1987). Our data show that, for 5 of 6 soils, this effect could sufficiently be explained by a mobilization of N stored in the biomass of the microflora. For example, the biomass reduction in the A. caliginosa treatments of Rendzina I at day 21 corresponds to a reduced microbial N immobilization of about 50 pg N gg ’ soil (assuming a C-to-N ratio of 6.5 for the soil microflora; cf. Anderson and Domsch, 1980). However, the increased biomass in the same soil at day 42 indicates that such conclusions should be drawn with great care. Under natural conditions, the short-term mobilization of N could be more than outbalanced by the long-term immobilization of N in ageing casts. These exemplary calculations, together with the discussion on microbial succession in the previous paragraphs, highlight the fact that the quantitative microbiological methods applied in our study can be used to link the results of descriptive microbiological methods to results from functional approaches. This approach may greatly help us to obtain a deeper insight into the complex biotic interactions in soil and to quantify the effects of soil invertebrates on microbial performance. Acknowledgements-We would like to thank Professor B. Meyer and Professor M. Schaefer for useful discussion and Martina Knaust and Monika Franke-Klein for their technical assistance. REFERENCES AK Bodensystematik (1985) Soil classification of the Federal Republic of Germany (abridged English version). Mitteilungen der Deutschen Bodenkundlichen Gesellschaft 44, l-96. Anderson J. M. (1988) The role of soil fauna in agricultural systems. In Advances in Nitrogen Cycling in Agricultural Ecosystems (J. R. Wilson, Ed.), pp. 89-113. CAB International, Wallingford. Anderson J. P. E. and Domsch K. H. (1980) Quantities of plant nutrients in the microbial biomass of selected soils. Soil Science 130,21 l-216. Atlavinyte O., Bagdonaviciene Z. and Budviciene L. (1968) The effect of Lumbricidae on the barley crops in various soils. Pedobiologia 8, 415-423. Edwards C. A. and Lofty J. R. (1977) Biology of Earthworms. Chapman & Hall, London. Heal 0. W. and Dighton J. (1985) Resource quality and

177

trophic structure in the soil system. In Ecological fnteractions in Soil (A. H. Fitter, Ed.), pp. 339-354, Blackwell,

Oxford. Jenkinson D. S. (1988) The determination of microbial biomass carbon and nitrogen in soil. In Advances in Nitrogen Cycling in Agricultural Ecosystems (J. A. Wilson, Ed.). DD. 368-386. CAB International, Wallinnford. Judas M. (1989) Populationsakologie her Reg&vilrmer (Lumbricidae) in einem Kalkbuchenwald: Abundanzdynamik und Bedeutung von Nahrungsressourcen. Berichte des Forschungszentrums Waldiikosyteme (A) 53, l-140. Koxlovskaya L. S. and Zhdannikova L. M. (1966) Relationships between earthworms and microbes in W. Siberia. Pedobiologia 6, 244-257. Lee K. E. (1985) Earthworms. Academic Press, Sydney. Marinissen J. C. Y. and Dexter A. R. (1990) Mechanisms of stabilization of earthworm casts and artificial casts. Biology and Fertility of Soils 9, 163-167. Nowak E. (1975) Population density of earthworms and some elements of their production in several grassland environments. Ekologia Polska 23, 459-491. Parle J. N. (1963) A microbiolonical study of earthworm casts. Journal of General MicrGbiology 3i, 13-23. Paul E. A. and Clark F. E. (1989) Soil hficrobiologv and Biochemistry. Academic Press, S’an Diego. -I Pirt S. J. (1975) Principles of Microbe and Cell Cultivation. Blackwell, Oxford. Ponomereva S. I. (1953) The influence of the activity of earthworms on the creation of stable structure in ley rotations. Pochvovedenie, 476-486. Salisbury E. J. (1925) The influence of earthworms on soil reaction and the stratification of natural soils. Journal of the Linnean Society (Bat.) 46, 415-425. Satchel1 J. E. (1983) Earthworm microbiology. In Earthworm Ecology (J. E. Satchel], Ed.), pp. 351-364. Chapman & Hall, London. Schaefer M. (1990) The soil fauna of a beech forest on limestone: trophic structure and energy budget. Oecologia 82, 128-136. Scheu S. (1987) Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae). Biology and Fertility of Soils 5, 230-234. Shaw C. and Pawluk S. (1986) Faecal microbiology of Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris and its relation to the carbon budget of three artificial soils. Pedobiologia 29, 377-389. Swift M. J. (1984) Microbial diversity and decomposer niches. In Current Perspectives in Microbial Ecology (M. J. Klug and C. A. Reddy, Eds), pp. 8-16. American Society of Microbiology, Washington DC. Uhich B. (1987) Stability, elasticity, and resilience of terrestrial ecosystems with respect to matter balance. In Potentials and Limitations of Ecosystem Analysis (E.-D. Schulxe and H. Zwlilfer, Eds), pp. 50-67. Springer, Berlin.1 Vance E. D., Brookes P. C. and Jenkinson D. S. (1987) An extraction method for measuring soil microbial C.. Soil Biolonv and Biochemistrv 19. 703-707. Walters?. (1983) Gkologische Untersuchungen an Collembolen eines Buchenwaldes auf Kalk. Pedobiologia 25, 73-85. Wolters V. (1989) The influence of omnivorous elaterid larvae on the microbial carbon cycle in different forest soils. Oecologia 80, 405-413. Wolters V. (1991) Biological processes in two beech forest soils treated with simulated acid rain-a laboratory experiment with Isotoma tigrina (Insecta:Collembola). Soil Biology & Biochemistry %3, 381-390. Wolters V. and Joeraensen R. G. (1991) Microbial carbon turnover in beech forest soils at different stages of acidification. Soil Biology & Biochemistry 23, 897-902. Wu J., Joergensen R. G., Pommerening B., Chaussod R. and Brookes P. C. (1990) Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biology & Biochemistry 22, 1167-1169. I.

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