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Changes in structure, organic matter and microbial activity in pine forest soil following the introduction of Dendrobaena octaedra (Oligochaeta, Lumbricidae)
Soil Biol. Biochem. Vol. 29, No. 3/4, pp. 537-540, 1997 0 1997 Elsevier Science Ltd. All rights reserved Printed in Great Britain PII: SOO38-0717(%)00178-2 003%0717/97 $17.00 + 0.00
CHANGES IN STRUCTURE, ORGANIC MATTER AND MICROBIAL ACTIVITY IN PINE FOREST SOIL FOLLOWING THE INTRODUCTION OF DENDROBAENA OCTAEDRA (OLIGOCHAETA, LUMBRICIDAE) M. A. MCLEAN* and D. PARKINSON Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada (Accepted 24 June 1996)
Summary-Epigeic earthworms [Dendrobaena octaedra (Savigny)] were introduced into intact litter-soil cores from a lodgepole pine forest. At three and six months following introduction of earthworms, changes in litter-soil structure, organic matter content (OM), basal respiration (BR) and microbial biomass (MB) were assessed. At six months 136f 173 and 430 f 235 ind. m-’ of D. octaedra were present in the low and high earthworm density treatments, respectively. Initial effects were seen in the H horizon where organic and mineral material were mixed. In the high density cores after six months the F and H layers were indistinguishable, consisting entirely of casts. At six months OM decreased significantly in the H layer at both earthworm densities and OM was significantly lower in the high density cores. BR and qC0, were not affected by earthworm density, but high earthworm density decreased MB in the F/H layer primarily due to the reduction in OM in this layer. @_I1997 Elsevier Science Ltd
INTRODUCTION Despite comprehensive soil samples over the previous six years, it was not until 1990 that earthworms were recorded sporadically in lodgepole pine forests in the Lusk Creek watershed, Kananaskis Valley, SW. Alberta. Recent surveys have shown the presence of significant numbers of the epigeic species Dendrobaenn octaedra (Savigny) in some pine forests in this area (Dymond et al., 1997). If significant changes in the organic soil horizons are caused by these invasions, they can be expected to have significant effects on soil biological activities. In a laboratory experiment using litter-soil cores from a lodgepole pine forest the effects of D. octaedra on the micromorphological diversity of the organic and upper mineral horizon and % organic matter content (OM), basal respiration (BR) and substrate-induced respiration (MB) in the organic and upper mineral horizons were examined.
METHODS AND MATERIALS
This experiment was conducted in mesocosms maintained at optimum temperature and moisture conditions for six months. These consisted of intact, undisturbed litter-soil cores 30 cm dia by 25 cm *Author for correspondence.
deep enclosed in galvanized sheet metal cylinders. Intact soil cores were collected in October 1993, and mesocosms were set up within four days of collection. Each mesocosm sat in a plastic tray containing 2 cm of damp sand (-19% wet wt) and was enclosed in a plastic bag sealed at the top around a foam plug to allow air movement and maintain moisture. Two treatments were used in this experiment: control cores to which no earthworms were added; and cores with D. octaedra added in numbers equivalent to a field density of 250 immatures and 70 matures m-* (S. Scheu, pers commun.). At three and six months, five replicates of each treatment were destructively sampled and the measurements outlined in Table 1 were made. Standard definitions of L, F, H, Ah and mineral material were used to distinguish the horizons (Green et al., 1993; Soil Science Society of America, 1987). OM and qCOz data were square root transformed and the BR and MB data were natural logarithm transformed before analysis in a repeated measures ANOVA. Since different horizons were present and sampled at the two dates, data were compared in two ways; the horizons present at both dates were compared at both dates and all the horizons at the second date were compared. 537
538
M. A. McLean and D. Parkinson Table 1. Parameters measured, soil horizons sampled (0, all organic layers; M, mineral), method and references
Parameter
Horizons
Method
References
worms
All 0, upper M All All All
Heat extraction Observation at 16x Loss on ignition IRGA - ~1 CO2 g-’ h-’ Substrate-induced respiration (IRGA - pl CO2 g-’ h-‘) 32,000 pg glucose g-’ 8000 pg glucose g-’ 2000 pg glucose g-1 pg CO,-C pg C ,: h-’
Abrahamson (1972) Nelson and Sommers (1982) Anderson ( 1982) Anderson and Domsch (1978)
Structure Organic matter (OM) Basal respiration (BR) Microbial biomass (MB)
F. H. F/H Ah M All
Metabolic quotient (qCO2)
RESULTS
Earthworm survival
Sampling at three months revealed that earthworms were already present in the control cores before the start of the experiment. At three months mean (*SD) numbers of earthworms me2 in the control and worm-treated cores were 147 _t 130 and 475 + 242 rnd2, respectively, and these were significantly different (P < 0.05). At six months there were 136 + 173 and 430 f 235 earthworms mm2 in the control and worm-treated cores, respectively, and these were significantly different (P < 0.05). Therefore, the treatments will be referred to as low density and high worm density, respectively. Structural changes
After three months, a small number of casts was seen in the H layer in the low density cores. In the high worm density cores the H layer was composed almost entirely of casts, casts were being deposited in the F layer, and a rudimentary Ah horizon was developing.
Anderson and Domsch (1985)
After six months, the H layer in low density cores was composed of many casts and a rudimentary Ah horizon was developing. In the high worm density cores, the F layer was much reduced, and in some cases eliminated. In these cores, a thick layer of casts lay between the L layer and the Ah horizon. The Ah horizon in these cores had increased in depth by a mean of 1.2 cm. Organic matter and microbial activity
At both dates, the H layer in the low density cores had a significantly higher OM than the high worm density cores (Table 2). In both treatments the OM of the H layer decreased significantly between three and six months. While the L and F layers had similar OM in the low density cores at three months, the F layer contained significantly less organic matter than the L layer at both dates in the high worm density cores. In both treatments OM decreased significantly with increasing depth at both dates. When BR was calculated on a total mass basis for each horizon no treatment or time effects were
Table 2. Mean organic matter content (OM) and microbial activity in soil horizons at three and six months after inoculation with D. octaedra(n = 5). Within columns, values followed by different letters are significantly different (P 5 0.05). Lower case letters refer to analyses of F/H and M at both three and six months. Capitals refer to analyses of all horizons at six months. ND, not determined since Ah not present at three months. F/H layer mixed by worms in high worm density cores at six months; otherwise mechanically mixed Parameter
Low worm density
Horizon 3
OM
BR pl CO* g-’ soil h-’
BRjO pl CO1 g-’ OM h-’
MB pg C,,, g-’ soil h-’
MB/O pg C,;, g-’ OM h-’
qCOzfigCO2 - C&Z
&h-l
L F H Ah
88’ 82’ 71b ND
M F/H Ah M F/H Ah M F/H Ah M F/H Ah M F/H Ah M
5’ 44” ND 2b 55 ND 34 7860’ ND 340b 9950” ND 7550b 0.0030 ND 0.0026
’ Significant difference between treatments within rows (P < 0.05). * Significant difference between dates within rows (P s 0.05).
High worm density 6
;;:: 54ba 19c llCD 28aA 2a lbB 42A 11; 592080”” 145oa 350k 8760aA 7570A 7210bA 0.0025A 0.0008a 0.0021*
3
6
88” 82b 60’
87aA 5gbA 44catz
ND 5d 24’ ND 2b 34 ND 32 6720” ND 26Qb 10120a ND 6310b 0.0019 ND 0.0033
22= qdD ‘F Ibe 46A 178 a &$A+
184Oa 380bC+ 8740UA :5%: 0.0028A 0.001 la 0.0021A
539
Earthworm effects on microbial activity found (Table 2). BR was significantly higher in F/H material than in mineral material at both dates. When BR was calculated on a mass of organic matter basis (BR/O) no significant differences were found between horizons except at six months when both BR and BR/O were higher in F/H material than in Ah and mineral material (Table 2). When calculated on a total mass basis, MB in F/ H and mineral horizons was higher in low density cores than in high worm density cores at both dates (Table 2). However, there was no significant difference between treatments when MB was calculated on a mass of organic matter basis (MB/O; Table 2). MB and MB/O were significantly higher in F/H material than in mineral material at both dates in both treatments. At six months MB decreased significantly with depth but there were no significant differences in MB/O (Table 2). Neither treatment nor date affected metabolic quotient (qCO2) (Table 2). At six months qCOz was significantly higher in F/H and mineral material than in Ah material (Table 2).
DKKXJSSION The initial effects of earthworms were evident in the low density cores at three months, in which earthworms were beginning to mix the H layer with some mineral material and casts were evident. At this stage, the OM of the L and F layers was not significantly different. The next stage was evident in the high worm density cores at three months; the H layer was composed almost entirely of casts, casts were beginning to be deposited in the F layer and the development of a rudimentary Ah horizon was observed. In this second stage, the OM of the H layer had decreased as had that of the F layer as casts were deposited in this layer. Following this, as shown in the high worm density cores at six months, the F and H layers were almost entirely composed of casts and were no longer distinguishable, and the OM content of this mixed layer had decreased relative to the original layers. Earthworm density did not affect BR. D. octaedra only marginally increased BR in spruce humus and birch litter microcosms (Haimi and Einbork, 1992; Haimi and Huhta, 1990). Ponge, 1991 observed that an epigeic species, probably D. octaedra, comminuted ingested material, but no transformation of plant or fungal material occurred during gut transit. It has been shown that comminution alone does not stimulate microbial respiration although the concentration of dissolved organic carbon in litter leachates is correlated with microbial respiration (Gunnarsson et al., 1988; Hassall et al., 1987). Both spruce and birch litter contain a higher content of labile materials than pine needles (Taylor et al., 1991), and therefore microbial respiration on these substrates would be higher than that on pine litter,
thus accounting for the differences seen between the present study and those of Haimi and Einbork, 1992 and Ha&i and Huhta, 1990. There are two possible explanations for the observed decrease in MB in the F/H and mineral horizons in the presence of high densities of earthworms: the decrease in OM content due to the mixing activities of the earthworms; and depression of fungal respiration due to mycelial disruption by earthworm activity. Since there were no significant differences in MB/O between treatments it appears that the decrease in MB in the F/H layer in the high worm density cores can be attributed to the decrease in OM content in this horizon. D. octaedra significantly reduced microbial biomass in aspen L/ F material and increased microbial biomass in aspen Ah material (Scheu and Parkinson, 1994). These results may also have been due to the decrease in OM in the organic horizons and an increase in OM in the mineral horizon, although this cannot be determined since OM content was not measured (Scheu and Parkinson, 1994). However, this does not explain the decrease in microbial biomass observed when D. octaedra was grown in pine F/H material alone (Scheu and Parkinson, 1994). Since fungi are the major component of microbial biomass in coniferous forest organic layers (Parkinson, 1988) effects of earthworms on fungal activity will have a significant effect on microbial activity and biomass. D. octaedra increased the bacterial contribution to microbial biomass in aspen L/ F and Ah horizons (Scheu and Parkinson, 1994). It appears that the burrowing activities of soil macrofauna including earthworms may depress fungal growth and microbial biomass presumably due to disruption of the fungal mycelium (Hanlon and Anderson, 1980; Parle, 1963; Wolters, 1989). This may be a contributing factor to the observed depression in MB in the high worm density cores. Metabolic quotient and BR/O were lower in the Ah horizon relative to the F/H layer at six months at both worm densities, suggesting that OM is less accessible to the microbes in the Ah horizon. This may be due to the stabilization of carbohydrate C through binding to clays which has been shown to occur in earthworm processed mineral soils (Shaw and Pawluk, 1986). Acknowledgements-The authors gratefully acknowledge the statistical advice of Dr L. Harder and the helpful comments of two anonymous reviewers on a previous draft. The work was supported by an NSERC operating grant to D. Parkinson.
REFERENCES Abrahamson G. (1972) Ecological study of Lubricidae (Oligochaeta) in Norwegian coniferous forest soils. Pedobiologia12, 267-28 1.
540
M. A. McLean and D. Parkinson
Anderson J. P. E. (1982) Soil Respiration. In Methodr of Soil Analysis. Part 2. Chemical and Microbiological Properties, 2nd edn (A. L. Page, R. H. Miller and D. R.
Keeney, Eds), pp. 831-871. American Society of Agronomy, Madison. Anderson J. P. E. and Domsch K. H. (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biology & Biochemistry 10, 215-221. Anderson T. H. and Domsch K. H. (1985) Maintenance carbon requirements of actively-metabolizing microbial populations under in situ conditions. Soil Biology & Biochemistry 17, 197-203.
Dymond P., Scheu S. and Parkinson D. (1997) Density and distribution of Dendrobaena octaedra (Lumbricidae) in an aspen and pine forest in the Canadian Rocky Mountains (Alberta). Soil Biology & Biochemistry 29, 265-273.
Green R. N., Trowbridge R. L. and Klinka K. (1993) Towards a taxonomic classification of humus forms. Forest Science Monograph 29.
Gunnarsson T., Sundin P. and Tunlid A. (1988) Importance of leaf litter fragmentation for bacterial growth. Oihos 52, 303-308. Haimi J. and Einhork M. (1992) Effects of endogeic earthworms on soil processes and plant growth in coniferous forest soil. Biology and Fertility of Soils 13, 6-10. Haimi J. and Huhta V. (1990) Effects of earthworms on decomposition processes in raw humus forest soil: a microcosm study. Biology and Fertility of Soils 10, 178183. Hanlon R. D. G. and Anderson J. M. (1980) Influence of macroarthropod feeding activities on microflora in decomposing oak leaves. Soil Biology & Biochemistry 12,255-261.
Hassall M., Turner J. G. and Rands M. R. W. (1987) Effects of terrestrial isopods on the decomposition of woodland leaf litter. Oecologia 72, 597-604. Nelson D. W. and Sommers L. E. (1982) Total carbon, organic carbon, and organic matter. In Methods of Soil Analysis. Parr 2. Chemical and Microbiological Properties, 2nd edn (A. L. Page, R. H. Miller and D. R.
Keeney, Eds), pp. 539-579. American Society of Agronomy, Madison. Parkinson D. (1988) Linkages between resource availability, microorganisms and soil invertebrates. Agriculture, Ecosystems and Environment 24, 21-32.
Parle J. N. (1963) A microbiological study of earthworm casts. Journal of General Microbiology 31, 13-22. Ponge J. F. (1991) Food resources and diets of soil animals in a small area of Scats pine litter. Geogerma 49, 33-62.
Scheu S. and Parkinson D. (1994) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms from cool temperate forests of the Canadian Rocky Mountains - laboratory studies. Applied Soil Ecology 1, 113-125. Shaw C. and Pawluk S. (1986) The development of soil structure by Octolasion tyrtaeum. Aporrectodea turgida and Lumbricus rerrestris in parent materials belonging to different textural classes. Pedobiologia 29, 327-339. Soil Science Society of America (1987) Glossary of Soil Science Terms, Soil Science Society of America, Madison. Taylor B. R., Prescott C. E., Parsons W. J. F. and Parkinson D. (1991) Substrate control of litter decomposition in four Rocky mountain coniferous forests. Canadian Journal of Botany 69, 2242-2250.
Wolters V. (1989) The influence of omnivorous elaterid larvae on the microbial carbon cycle in different forest soils. Oecologia 80, 405413.
CHANGES IN STRUCTURE, ORGANIC MATTER AND MICROBIAL ACTIVITY IN PINE FOREST SOIL FOLLOWING THE INTRODUCTION OF DENDROBAENA OCTAEDRA (OLIGOCHAETA, LUMBRICIDAE) M. A. MCLEAN* and D. PARKINSON Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada (Accepted 24 June 1996)
Summary-Epigeic earthworms [Dendrobaena octaedra (Savigny)] were introduced into intact litter-soil cores from a lodgepole pine forest. At three and six months following introduction of earthworms, changes in litter-soil structure, organic matter content (OM), basal respiration (BR) and microbial biomass (MB) were assessed. At six months 136f 173 and 430 f 235 ind. m-’ of D. octaedra were present in the low and high earthworm density treatments, respectively. Initial effects were seen in the H horizon where organic and mineral material were mixed. In the high density cores after six months the F and H layers were indistinguishable, consisting entirely of casts. At six months OM decreased significantly in the H layer at both earthworm densities and OM was significantly lower in the high density cores. BR and qC0, were not affected by earthworm density, but high earthworm density decreased MB in the F/H layer primarily due to the reduction in OM in this layer. @_I1997 Elsevier Science Ltd
INTRODUCTION Despite comprehensive soil samples over the previous six years, it was not until 1990 that earthworms were recorded sporadically in lodgepole pine forests in the Lusk Creek watershed, Kananaskis Valley, SW. Alberta. Recent surveys have shown the presence of significant numbers of the epigeic species Dendrobaenn octaedra (Savigny) in some pine forests in this area (Dymond et al., 1997). If significant changes in the organic soil horizons are caused by these invasions, they can be expected to have significant effects on soil biological activities. In a laboratory experiment using litter-soil cores from a lodgepole pine forest the effects of D. octaedra on the micromorphological diversity of the organic and upper mineral horizon and % organic matter content (OM), basal respiration (BR) and substrate-induced respiration (MB) in the organic and upper mineral horizons were examined.
METHODS AND MATERIALS
This experiment was conducted in mesocosms maintained at optimum temperature and moisture conditions for six months. These consisted of intact, undisturbed litter-soil cores 30 cm dia by 25 cm *Author for correspondence.
deep enclosed in galvanized sheet metal cylinders. Intact soil cores were collected in October 1993, and mesocosms were set up within four days of collection. Each mesocosm sat in a plastic tray containing 2 cm of damp sand (-19% wet wt) and was enclosed in a plastic bag sealed at the top around a foam plug to allow air movement and maintain moisture. Two treatments were used in this experiment: control cores to which no earthworms were added; and cores with D. octaedra added in numbers equivalent to a field density of 250 immatures and 70 matures m-* (S. Scheu, pers commun.). At three and six months, five replicates of each treatment were destructively sampled and the measurements outlined in Table 1 were made. Standard definitions of L, F, H, Ah and mineral material were used to distinguish the horizons (Green et al., 1993; Soil Science Society of America, 1987). OM and qCOz data were square root transformed and the BR and MB data were natural logarithm transformed before analysis in a repeated measures ANOVA. Since different horizons were present and sampled at the two dates, data were compared in two ways; the horizons present at both dates were compared at both dates and all the horizons at the second date were compared. 537
538
M. A. McLean and D. Parkinson Table 1. Parameters measured, soil horizons sampled (0, all organic layers; M, mineral), method and references
Parameter
Horizons
Method
References
worms
All 0, upper M All All All
Heat extraction Observation at 16x Loss on ignition IRGA - ~1 CO2 g-’ h-’ Substrate-induced respiration (IRGA - pl CO2 g-’ h-‘) 32,000 pg glucose g-’ 8000 pg glucose g-’ 2000 pg glucose g-1 pg CO,-C pg C ,: h-’
Abrahamson (1972) Nelson and Sommers (1982) Anderson ( 1982) Anderson and Domsch (1978)
Structure Organic matter (OM) Basal respiration (BR) Microbial biomass (MB)
F. H. F/H Ah M All
Metabolic quotient (qCO2)
RESULTS
Earthworm survival
Sampling at three months revealed that earthworms were already present in the control cores before the start of the experiment. At three months mean (*SD) numbers of earthworms me2 in the control and worm-treated cores were 147 _t 130 and 475 + 242 rnd2, respectively, and these were significantly different (P < 0.05). At six months there were 136 + 173 and 430 f 235 earthworms mm2 in the control and worm-treated cores, respectively, and these were significantly different (P < 0.05). Therefore, the treatments will be referred to as low density and high worm density, respectively. Structural changes
After three months, a small number of casts was seen in the H layer in the low density cores. In the high worm density cores the H layer was composed almost entirely of casts, casts were being deposited in the F layer, and a rudimentary Ah horizon was developing.
Anderson and Domsch (1985)
After six months, the H layer in low density cores was composed of many casts and a rudimentary Ah horizon was developing. In the high worm density cores, the F layer was much reduced, and in some cases eliminated. In these cores, a thick layer of casts lay between the L layer and the Ah horizon. The Ah horizon in these cores had increased in depth by a mean of 1.2 cm. Organic matter and microbial activity
At both dates, the H layer in the low density cores had a significantly higher OM than the high worm density cores (Table 2). In both treatments the OM of the H layer decreased significantly between three and six months. While the L and F layers had similar OM in the low density cores at three months, the F layer contained significantly less organic matter than the L layer at both dates in the high worm density cores. In both treatments OM decreased significantly with increasing depth at both dates. When BR was calculated on a total mass basis for each horizon no treatment or time effects were
Table 2. Mean organic matter content (OM) and microbial activity in soil horizons at three and six months after inoculation with D. octaedra(n = 5). Within columns, values followed by different letters are significantly different (P 5 0.05). Lower case letters refer to analyses of F/H and M at both three and six months. Capitals refer to analyses of all horizons at six months. ND, not determined since Ah not present at three months. F/H layer mixed by worms in high worm density cores at six months; otherwise mechanically mixed Parameter
Low worm density
Horizon 3
OM
BR pl CO* g-’ soil h-’
BRjO pl CO1 g-’ OM h-’
MB pg C,,, g-’ soil h-’
MB/O pg C,;, g-’ OM h-’
qCOzfigCO2 - C&Z
&h-l
L F H Ah
88’ 82’ 71b ND
M F/H Ah M F/H Ah M F/H Ah M F/H Ah M F/H Ah M
5’ 44” ND 2b 55 ND 34 7860’ ND 340b 9950” ND 7550b 0.0030 ND 0.0026
’ Significant difference between treatments within rows (P < 0.05). * Significant difference between dates within rows (P s 0.05).
High worm density 6
;;:: 54ba 19c llCD 28aA 2a lbB 42A 11; 592080”” 145oa 350k 8760aA 7570A 7210bA 0.0025A 0.0008a 0.0021*
3
6
88” 82b 60’
87aA 5gbA 44catz
ND 5d 24’ ND 2b 34 ND 32 6720” ND 26Qb 10120a ND 6310b 0.0019 ND 0.0033
22= qdD ‘F Ibe 46A 178 a &$A+
184Oa 380bC+ 8740UA :5%: 0.0028A 0.001 la 0.0021A
539
Earthworm effects on microbial activity found (Table 2). BR was significantly higher in F/H material than in mineral material at both dates. When BR was calculated on a mass of organic matter basis (BR/O) no significant differences were found between horizons except at six months when both BR and BR/O were higher in F/H material than in Ah and mineral material (Table 2). When calculated on a total mass basis, MB in F/ H and mineral horizons was higher in low density cores than in high worm density cores at both dates (Table 2). However, there was no significant difference between treatments when MB was calculated on a mass of organic matter basis (MB/O; Table 2). MB and MB/O were significantly higher in F/H material than in mineral material at both dates in both treatments. At six months MB decreased significantly with depth but there were no significant differences in MB/O (Table 2). Neither treatment nor date affected metabolic quotient (qCO2) (Table 2). At six months qCOz was significantly higher in F/H and mineral material than in Ah material (Table 2).
DKKXJSSION The initial effects of earthworms were evident in the low density cores at three months, in which earthworms were beginning to mix the H layer with some mineral material and casts were evident. At this stage, the OM of the L and F layers was not significantly different. The next stage was evident in the high worm density cores at three months; the H layer was composed almost entirely of casts, casts were beginning to be deposited in the F layer and the development of a rudimentary Ah horizon was observed. In this second stage, the OM of the H layer had decreased as had that of the F layer as casts were deposited in this layer. Following this, as shown in the high worm density cores at six months, the F and H layers were almost entirely composed of casts and were no longer distinguishable, and the OM content of this mixed layer had decreased relative to the original layers. Earthworm density did not affect BR. D. octaedra only marginally increased BR in spruce humus and birch litter microcosms (Haimi and Einbork, 1992; Haimi and Huhta, 1990). Ponge, 1991 observed that an epigeic species, probably D. octaedra, comminuted ingested material, but no transformation of plant or fungal material occurred during gut transit. It has been shown that comminution alone does not stimulate microbial respiration although the concentration of dissolved organic carbon in litter leachates is correlated with microbial respiration (Gunnarsson et al., 1988; Hassall et al., 1987). Both spruce and birch litter contain a higher content of labile materials than pine needles (Taylor et al., 1991), and therefore microbial respiration on these substrates would be higher than that on pine litter,
thus accounting for the differences seen between the present study and those of Haimi and Einbork, 1992 and Ha&i and Huhta, 1990. There are two possible explanations for the observed decrease in MB in the F/H and mineral horizons in the presence of high densities of earthworms: the decrease in OM content due to the mixing activities of the earthworms; and depression of fungal respiration due to mycelial disruption by earthworm activity. Since there were no significant differences in MB/O between treatments it appears that the decrease in MB in the F/H layer in the high worm density cores can be attributed to the decrease in OM content in this horizon. D. octaedra significantly reduced microbial biomass in aspen L/ F material and increased microbial biomass in aspen Ah material (Scheu and Parkinson, 1994). These results may also have been due to the decrease in OM in the organic horizons and an increase in OM in the mineral horizon, although this cannot be determined since OM content was not measured (Scheu and Parkinson, 1994). However, this does not explain the decrease in microbial biomass observed when D. octaedra was grown in pine F/H material alone (Scheu and Parkinson, 1994). Since fungi are the major component of microbial biomass in coniferous forest organic layers (Parkinson, 1988) effects of earthworms on fungal activity will have a significant effect on microbial activity and biomass. D. octaedra increased the bacterial contribution to microbial biomass in aspen L/ F and Ah horizons (Scheu and Parkinson, 1994). It appears that the burrowing activities of soil macrofauna including earthworms may depress fungal growth and microbial biomass presumably due to disruption of the fungal mycelium (Hanlon and Anderson, 1980; Parle, 1963; Wolters, 1989). This may be a contributing factor to the observed depression in MB in the high worm density cores. Metabolic quotient and BR/O were lower in the Ah horizon relative to the F/H layer at six months at both worm densities, suggesting that OM is less accessible to the microbes in the Ah horizon. This may be due to the stabilization of carbohydrate C through binding to clays which has been shown to occur in earthworm processed mineral soils (Shaw and Pawluk, 1986). Acknowledgements-The authors gratefully acknowledge the statistical advice of Dr L. Harder and the helpful comments of two anonymous reviewers on a previous draft. The work was supported by an NSERC operating grant to D. Parkinson.
REFERENCES Abrahamson G. (1972) Ecological study of Lubricidae (Oligochaeta) in Norwegian coniferous forest soils. Pedobiologia12, 267-28 1.
540
M. A. McLean and D. Parkinson
Anderson J. P. E. (1982) Soil Respiration. In Methodr of Soil Analysis. Part 2. Chemical and Microbiological Properties, 2nd edn (A. L. Page, R. H. Miller and D. R.
Keeney, Eds), pp. 831-871. American Society of Agronomy, Madison. Anderson J. P. E. and Domsch K. H. (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biology & Biochemistry 10, 215-221. Anderson T. H. and Domsch K. H. (1985) Maintenance carbon requirements of actively-metabolizing microbial populations under in situ conditions. Soil Biology & Biochemistry 17, 197-203.
Dymond P., Scheu S. and Parkinson D. (1997) Density and distribution of Dendrobaena octaedra (Lumbricidae) in an aspen and pine forest in the Canadian Rocky Mountains (Alberta). Soil Biology & Biochemistry 29, 265-273.
Green R. N., Trowbridge R. L. and Klinka K. (1993) Towards a taxonomic classification of humus forms. Forest Science Monograph 29.
Gunnarsson T., Sundin P. and Tunlid A. (1988) Importance of leaf litter fragmentation for bacterial growth. Oihos 52, 303-308. Haimi J. and Einhork M. (1992) Effects of endogeic earthworms on soil processes and plant growth in coniferous forest soil. Biology and Fertility of Soils 13, 6-10. Haimi J. and Huhta V. (1990) Effects of earthworms on decomposition processes in raw humus forest soil: a microcosm study. Biology and Fertility of Soils 10, 178183. Hanlon R. D. G. and Anderson J. M. (1980) Influence of macroarthropod feeding activities on microflora in decomposing oak leaves. Soil Biology & Biochemistry 12,255-261.
Hassall M., Turner J. G. and Rands M. R. W. (1987) Effects of terrestrial isopods on the decomposition of woodland leaf litter. Oecologia 72, 597-604. Nelson D. W. and Sommers L. E. (1982) Total carbon, organic carbon, and organic matter. In Methods of Soil Analysis. Parr 2. Chemical and Microbiological Properties, 2nd edn (A. L. Page, R. H. Miller and D. R.
Keeney, Eds), pp. 539-579. American Society of Agronomy, Madison. Parkinson D. (1988) Linkages between resource availability, microorganisms and soil invertebrates. Agriculture, Ecosystems and Environment 24, 21-32.
Parle J. N. (1963) A microbiological study of earthworm casts. Journal of General Microbiology 31, 13-22. Ponge J. F. (1991) Food resources and diets of soil animals in a small area of Scats pine litter. Geogerma 49, 33-62.
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