Introduction of the epigeic earthworm Dendrobaena octaedra changes the oribatid community and microarthropod abundances in a pine forest

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1 Soil Biology & Biochemistry 32 (2000) 1671± Introduction of the epigeic earthworm Dendrobaena octaedra changes the oribatid community and microarthropod abundances in a pine forest M.A. McLean*, D. Parkinson Department of Biological Sciences, University of Calgary, Calgary, AB, Canada T2N 1N4 Accepted 5 April 2000 Abstract The e ects of the activities of the epigeic earthworm Dendrobaena octaedra on the oribatid community and microarthropod abundances were studied in a 90-year old pine forest over 2 years. Oribatids were extracted from the L and FH layers and the A h and B m horizons at 1 and 2 years and data were analyzed using principal component analysis (PCA). High worm biomass correlated positively with oribatid species richness and diversity in the L layer. In the FH layer, worm biomass accounted for 83% of the variation in the oribatid community data and correlated negatively with oribatid species richness. High worm biomass correlated with decreases in the abundances of 18 oribatid species, and the total abundances of adult and juvenile oribatids, astigmatids, mesostigmatids, Actinedida and Arthropleona in the FH layer. These e ects were attributed to the changes in the physical structure of the organic layers of the soil. In the A h and B m horizons the C±N ratio accounted for 72± 97% of the variation in the oribatid species and microarthropod group data. The abundances of O. nova, other Oppioidea, several Brachychthoniidae, C. cuspidatus and adult (in the A h horizon only) and juvenile oribatids, and Arthropleona were positively correlated with the C±N ratio. This re ected the mixing of less decomposed organic matter into the lower horizons by D. octaedra Elsevier Science Ltd. All rights reserved. Keywords: Dendrobaena octaedra; Earthworm invasion; Oribatid community; Microarthropods 1. Introduction There is con icting evidence of the e ects of earthworms on soil microarthropods (arthropods between 200 mm and 2 mm, including mites and Collembola). Increased microarthropod abundance and diversity (Marinissen and Bok, 1988; Loranger et al., 1998), decreased abundance (Dash et al., 1980; Yeates, 1981) and mixed e ects (Yeates, 1981; Hamilton and Sillman, 1989; McLean and Parkinson, 1998; Maraun et al., 1999) have all been reported. Mechanisms which * Corresponding author. Louis Calder Center, Fordham University, 53 Whippoorwill Road, Armonk, NY 10504, USA. Tel.: X 18; fax: address: mclean@murray.fordham.edu (M.A. McLean). have been invoked to explain these e ects have included: (1) alteration in the physical structure of the soil (Marinissen and Bok, 1988; Hamilton and Sillman, 1989; Loranger et al., 1998; McLean and Parkinson, 1998; Maraun et al., 1999); (2) alteration of the chemical or physical characteristics of organic matter (OM) and its e ects on the soil microbes (Yeates, 1981; Hamilton and Sillman, 1989; Loranger et al., 1998; Maraun et al., 1999); (3) competition for food (Brown, 1995); and (4) predation (Dash et al., 1980). Some of the discrepancies between these studies are undoubtedly due to the di ering e ects of earthworms of di erent ecological strategy on soil physical structure and OM dynamics. Feeding of anecic earthworms (larger litter feeding species with permanent vertical burrows) increases the organic matter content and porosity of mull soils, and therefore might be expected /00/$ - see front matter Elsevier Science Ltd. All rights reserved. PII: S (00)

2 1672 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 to improve the physical and chemical characteristics of the soil for microarthropods. However, feeding by epigeic earthworms (smaller litter feeding species con ned to the organic and upper mineral layers) mixes mineral material into the organic layers, and might be expected to reduce physical and chemical soil qualities for microarthropods in the organic layers of the soil. Given the paucity of data on the e ects of earthworms on soil microarthropods and the di culties of arriving at any conclusions based on soils in which earthworms have previously been active, we were fortunate to be able to study the recent invasion of the epigeic earthworm Dendrobaena octaedra into lodgepole pine forest in SW Alberta, Canada. We used two approaches: short-term (6 months) laboratory studies (McLean and Parkinson, 1997a, 1998), and longer term (2 years) eld studies (McLean and Parkinson, 1997b, 2000, the present study). Under conditions of optimum moisture and temperature in mesocosms (intact soil cores 30 cm diameter 25 cm high), the activities of D. octaedra increased oribatid diversity and abundances (McLean and Parkinson, 1998). This was attributed to an increase in spatial heterogeneity through the addition of casts to the organic materials already present. However, since organic layers in the mesocosms with the highest worm numbers were completely homogenized at the end of 6 months, we hypothesized that the longer term (2 years) e ects of D. octaedra would be decreased oribatid diversity and microarthropod abundance. 2. Materials and methods 2.1. Site description The site of this experiment was a 90-year old lodgepole pine (Pinus contorta var. latifolia Engelm.) forest in the Kananaskis Valley of SW Alberta, Canada. For a more detailed description see McLean and Parkinson (1997b) Experimental design Five pairs of plots 1 m 2 m were set up in August 1993 in a part of the lodgepole pine forest which surveys had shown to be free from earthworms. Within each pair of plots, two treatments (control without earthworms and treatment with worms) were randomly assigned. The epigeic earthworm Dendrobaena octaedra (Savigny) was added to the worm plots at numbers equivalent to its 1993 eld density of 250 immatures and 70 matures m 2, with a total biomass of 3.3 g d wt m 2. The earthworms used were heat extracted (Kempson et al., 1963) from pine forest oor in a part of the forest where earthworms had already been established for a few years. In September 1994 and September 1995 the plots were sampled for microarthropod abundances and for assessment of worm abundance and biomass Earthworm abundance and biomass At each sampling time one core 10.5 cm diameter was taken from each plot and the earthworms present were heat extracted (Kempson et al., 1963) and counted as small (<10 mm long) immature, large immature, mature and aclitellate adults. Oven dry weights of each of the worm size classes were used to obtain estimates of worm biomass at each of the sampling times. Mean biomass of a mature worm was 27 mg DW Microarthropod abundances At each of the sampling times one core 5.5 cm diameter was taken from each plot to assess microarthropod abundances. Cores were separated into L and FH layers and into A h and B m horizons where possible and the microarthropods were heat extracted using a high gradient extractor (Merchant and Crossley, 1970) from each layer and horizon. Microarthropods were preserved in 70% ethanol and identi ed: adult oribatid to species where possible; juvenile oribatids to genus where possible; other mites and Collembola to suborder. Due to the heterogeneity of the soil and the presence of rocks, some samples did not include the B m horizon. Due to worm activities, an A h horizon developed in some plots but not in others, and was therefore not sampled in all cases. Oribatid community parameters (species richness (S ), dominance (d ), diversity (1/D )) were calculated from the abundance data for all horizons in all plots Statistical analysis At the time the plots were set up, earthworms were already invading the forest and therefore some of the ``control'' plots contained earthworms (McLean and Parkinson, 1997b) so nal earthworm biomass was included in the analysis. Data were analyzed using ordination which allows the simultaneous analysis of the whole community. Principal Components Analysis (PCA), a linear and indirect ordination method was chosen since (i) the range of sample scores was low, making a linear method preferable to a unimodal method, (ii) indirect ordination methods allow the discovery of the largest variation in the species data without being constrained by possibly irrelevant environmental variables, and (iii) analysis can be followed by correlation of the extracted axes with en-

3 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671± Table 1 Mean (standard error) oribatid species richness, dominance (d ), diversity (1/D ) and number of adult oribatids identi ed to species in the L and FH layers and the A h and B m horizons n ˆ 20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times L FH A h B m Richness 1.6 (1.5) 12.9 (5.8) 5.6 (3.4) 4.1 (3.1) d 0.62 (0.40) 0.42 (0.14) 0.67 (0.23) 0.60 (0.27) 1/D 1.79 (3.71) 5.00 (2.62) 2.85 (1.91) 3.41 (2.64) Number of Individuals 3 (3) 136 (122) 51 (56) 17 (17) vironmental variables to discover which, if any, of the supplied environmental variables (in this case, nal worm biomass, organic matter content (OM), moisture content, ph, C±N ratio) account for a signi cant proportion of the variation in the species data (ter Braak, 1995). Since the conditions in each soil layer/horizon were di erent, the analysis was conducted on each layer/horizon separately. 3. Results 3.1. Earthworm numbers and biomass Earthworm numbers ranged from 0 to 3349 individuals m 2, with a mean of 854 individuals m 2. Earthworm biomass ranged from 0 to 39.9 g DW m 2, with a mean of 8.3 g DW m 2. Fig. 1. PCA of oribatid community characteristics in the L layer in plots 1 and 2 year after the introduction of D. octaedra n ˆ 20). Codes are as follows; WORM WT nal worm biomass; H 2 O moisture content; BP Berger-Parker Index of Dominance; RICH species richness; IS Inverse Simpson Index of Diversity.

4 1674 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671± E ects on oribatid community structure Number of individuals, species richness and diversity were highest and dominance was lowest in the FH layer (Table 1). In the L layer, moisture content p < 0:01 and nal worm biomass p < 0:05 correlated with the rst PCA axis, accounting for 99% of the variation in oribatid community parameters (Fig. 1). In this layer both moisture content and worm biomass correlated positively with diversity and richness and negatively with dominance. In the FH layer, nal worm biomass p < 0:05 correlated with the rst PCA axis, accounting for 83% of the variation in oribatid community parameters (Fig. 2). In this layer nal worm biomass correlated negatively with richness. In the A h horizon, neither initial treatment nor nal worm biomass correlated with the extracted PCA axes, however moisture content correlated p < 0:05 with the second PCA axis, accounting for 19% of the variation in oribatid community parameters (data not shown). Moisture content correlated positively with diversity and negatively with dominance. In the B m horizon, nal worm biomass p < 0:05 and ph p < 0:05 correlated with the rst PCA axis, accounting for 63% of the variation in oribatid community parameters (data not shown). In this layer worm biomass correlated positively with oribatid dominance and negatively with richness, while ph correlated positively with richness and negatively with dominance E ects on oribatid species abundances In the course of this investigation, 55 oribatid species were extracted from the plots, many of which were observed only once. Mean abundances of the 20 most common species are listed in Table 2. In the L layer, none of the supplied environmental variables correlated with any of the PCA axes (data not shown). Fig. 2. PCA of oribatid community characteristics in the FH layer in plots 1 and 2 year after the introduction of D. octaedra n ˆ 22). Codes are as follows; WORM WT nal worm biomass; BP Berger-Parker Index of Dominance; RICH species richness; IS Inverse Simpson Index of Diversity.

5 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671± Table 2 Mean (standard error) raw abundances of oribatid species in the L and FH layers and the A h and B m horizons n ˆ 20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times L FH A h B m Paleacarus nr hystricinus TraÈ gaê rdh 0 (0) 5 (10) 0 (0) 0 (0) Liochthonius nr lapponicus(traè gaê rdh) 0 (0) 3 (5) 0 (0) 0 (0) Liochthonius simplex (Forsslund) 0 (1) 3 (6) 1 (1) 0 (0) Liochthonius sp 1 0 (0) 2 (3) 0 (0) 0 (0) Liochthonius sp 2 0 (0) 12 (28) 1 (2) 1 (1) Liochthonius sp 4 0 (0) 2 (3) 0 (1) 1 (2) Liochthonius sp 5 0 (0) 1 (2) 0 (0) 0 (1) Neoliochthonius sp 1 0 (0) 3 (5) 0 (1) 0 (0) Sellnickochthonius immaculatus Forsslund 0 (0) 3 (4) 0 (0) 0 (0) Sellnickochthonius suecicus Forsslund 0 (0) 11 (28) 2 (5) 1 (4) Oppiella nova (Oudemans) 0 (0) 26 (36) 34 (52) 7 (13) Quadroppia quadricarinata (Michael) 0 (0) 3 (6) 0 (0) 0 (0) Parisuctobelba sp 1 1 (2) 29 (54) 5 (7) 2 (3) Suctobelba sp 1 0 (0) 2 (5) 1 (1) 0 (0) Suctobelbella sp 1 0 (0) 1 (3) 0 (1) 0 (0) Suctobelbella sp 2 0 (0) 2 (3) 1 (1) 0 (0) Suctobelbella sp 3 0 (0) 4 (8) 0 (1) 0 (0) Ceratozetes gracilis (Michael) 0 (0) 7 (16) 1 (2) 0 (0) Ceratozetes sp 1 0 (1) 8 (12) 2 (3) 0 (1) Diapterobates humeralis (Hermann) 0 (0) 5 (12) 0 (0) 1 (2) In the FH layer, moisture content p < 0:01 correlated with the rst PCA axis and nal worm biomass p < 0:05 correlated with the second PCA axis, accounting for 56% and 28% of the variation in the oribatid species data, respectively (Fig. 3). Moisture content was positively correlated with Tectocepheus velatus, Diapterobates humeralis, Belba 2, Ceratozetes 1, Paleacarus 1, Trhypochthonius tectorum, Suctobelba 1, Ceratozetes gracilis, Parisuctobelba 1, Autogneta 1, Synchthonius crenulatus, Sy. elegans, Dyobelba 1, Brachychthonius bimaculatus and negatively correlated with Liochthonius spp 1, 2 and 4, O. clavigera, Liochthonius nr lapponicus, L. nr simplex, Neoliochthonius 1, O. nova, Suctobelbella spp 1, 2, 3, 5 and 6. Final worm biomass was negatively correlated with Table 3 Mean (standard error) raw abundances of adult and juvenile oribatids, Actinedida, astigmatids, mesostigmatids, tarsonemids, Arthropleona, and Symphypleona in the L and FH layers and in the A h and B m horizons n ˆ 20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times L FH A h B m Juvenile oribatids 4 (4) 31 (33) 17 (22) 6 (8) Adult oribatids 2 (3) 148 (129) 55 (57) 20 (17) Actinedida 2 (2) 21 (19) 13 (10) 6 (5) Astigmatids 0 (0) 21 (34) 3 (8) 3 (4) Mesostigmatids 1 (1) 32 (21) 7 (5) 3 (4) Tarsonemids 4 (7) 9 (10) 1 (1) 0 (1) Arthropleona 1 (2) 41 (31) 15 (8) 7 (7) Symphypleona 0 (0) 1 (1) 0 (0) 0 (0) Sellnickochthonius immaculata, Sy. elegans, Sy. crenulatus, Autogneta 1, C. gracilis, Parisuctobelba 1, Suctobelba 1, Paleacarus 1, Suctobelbella 1, 2, 3 and 6, Liochthonius 2, O. nova, Neoliochthonius 1, L. lapponicus, S. suecica, L. nr simplex. In the A h and B m horizons, neither the initial treatment nor nal worm biomass correlated signi cantly with any PCA axes. The C±N ratio p < 0:05, p < 0:05 correlated with the rst PCA axis, accounting for 97% and 78% of the variation in the oribatid species data, in the A h and B m horizons, respectively. In the A h horizon, C±N ratio correlated positively with O. nova, O. clavigera, C. cuspidatus, Dyobelba 1, Suctobelbella 2and4, Liochthonius 2, Sy. elegans, S. immaculatus, Q. quadricarinata and negatively with D. humeralis, Paleacarus 1, and Suctobelba 1 (Fig. 4). In the B m horizon, the C±N ratio correlated positively with O. nova, Liochthonius 1and5, L. nr simplex, L. nr lapponicus, Eueremaeus tetrosus, S. immaculatus, B. impressus, Suctobelbella 1, C. cuspidatus and correlated negatively with D. humeralis and Parisuctobelba 1 (data not shown) E ects on microarthropod abundances The total abundances of mites and Collembola extracted at 1 year were equivalent to 174,100 and 28,000 m 2, respectively. At 2 years the abundances were 134,900 and 28,800 m 2, respectively. Abundances of microarthropods were highest in the FH layer followed by the A h horizon (Table 3). In the L layer C±N ratio correlated p < 0:05 with

6 1676 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 the rst PCA axis and moisture content correlated p < 0:05 with the second PCA axis, accounting for 65% and 16% of the variation in the microarthropod abundances, respectively (data not shown). C±N ratio correlated positively with the abundance of tarsonemids and negatively with the abundances of adult oribatids, mesostigmatids and Arthropleona. Moisture content correlated positively with the abundance of adult and juvenile oribatids, mesostigmatids, Symphypleona and Actinedida. In the FH layer, nal worm biomass correlated p < 0:05 with the rst PCA axis, accounting for 88% of the variation in microarthropod abundances (Fig. 5). Final worm biomass correlated positively with the abundances of Symphypleona and negatively with the abundances of adult and juvenile oribatids, Actinedida, astigmatids, mesostigmatids and Arthropleona. In the A h and B m horizons, the C±N ratio correlated p < 0:05 with the rst PCA axis, accounting for 89% and 72% of the variation in microarthropod abundances, respectively. In the A h horizon, C±N ratio correlated positively with the abundances of adult and juvenile oribatids, Arthropleona, astigmatids, mesostigmatids and Actinedida and negatively with Symphypleona (Fig. 6). In the B m horizon, C±N ratio correlated positively with the abundances of juvenile oribatids, tarsonemids, astigmatids, mesostigmatids, Arthropleona and Actinedida (data not shown). Fig. 3. PCA of oribatid species in the FH layer in plots 1 and 2 year after the introduction of D. octaedra n ˆ 22). Codes as follows: H 2 O moisture content; WORM WT nal worm biomass; a1 Autogneta sp 1; bb Brachychthonius bimaculatus; bi Brachychthonius impressus; cc Ceratozetes cuspidatus; cg C. gracilis; c1 Ceratozetes sp 1; dh Diapterobates humeralis and Belba sp 2; dr Dentizetes rudentiger; ea Eremaeus translamellatus; eb Eobrachychthonius borealis?; el Epidamaeus longitarsalis; em Eueremaeus marshalli; er Eupterotegaeus rostratus; es Eueremaeus sp 1; et Eueremaeus tetrosus; e1 Epidamaeus sp 1; e3 Epidamaeus sp 3; ll Liochthonius nr lapponicus; l1 Liochthonius sp 1; l2 Liochthonius sp 2, Liochthonius nr simplex, Sellnickochthonius suecicus and Suctobelbella sp 6; l4 Liochthonius sp 4; l5 Liochthonius sp 5; mm Microppia minus; n1 Neoliochthonius sp 1; on O. nova; pa Paleacarus nr hystricinus; p1 Parisuctobelba sp 1; qq Quadroppia quadricarinata; q1 Quatrobelba sp 1; sb Suctobelba sp 1; sc Synchthonius crenulatus; se Synchthonius elegans; si Sellnickochthonius immaculatus; s1 Suctobelbella sp 1; s2 Suctobelbella sp 2 and Oppiella clavigera; s3 Suctobelbella sp 3; s4 Suctobelbella sp 4; tt Trhypochthonius tectorum; tv Tectocepheus velatus; t1 Tectocepheus sp 1.

7 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671± Discussion Two important ways in which epigeic earthworm feeding di ers from that of anecic and endogeic earthworms are that epigeics feed mainly on relatively undecomposed litter, while anecics and endogeics feed mainly on partially decomposed and highly decomposed organic materials, respectively (Daniel and Anderson, 1992; Edwards and Bohlen, 1996), and that epigeic gut passage results in comminuted but not transformed organic materials (Ponge, 1991; Daniel and Anderson, 1992; Ziegler and Zech, 1992; Edwards and Bohlen, 1996), while endogeic and anecic gut passage results in intimate mixing of mineral and transformed organic materials resulting in the welldocumented e ects on C and N in these casts (e.g. Edwards and Bohlen, 1996). Epigeic earthworm feeding activities may a ect the soil microarthropods through changes in the structure of the soil organic layers, through the impacts of comminution on their microbial food sources, or through competition for microbial food resources, and predation. There is evidence that oribatid species, although feeding on similar substrates, di er su ciently in size to be able to exploit di erent sized pores in organic soil layers, and therefore may be spatially separated (Anderson, 1978; Walter and Norton, 1984). In a detailed analysis of the relationship between microhabitat diversity and oribatid diversity, Anderson (1978) observed strong correlations between oribatid diversity and inter- and intra-habitat diversity. In our study, prior to earthworm invasion, the lodgepole pine forest oor consisted of well di erentiated L and F layers and a thin (1±2 cm) H layer above a B m horizon. Organic materials in these layers are quite distinct physically and chemically, and provide a variety of microhabitats for microarthropods (e.g. Berg et al., 1998). In year 2, in the two plots with the highest Fig. 4. PCA of oribatid species in the A h horizon in plots 1 and 2 year after the introduction of D. octaedra n ˆ 13). Codes as follows: C/N C± N ratio; cc Ceratozetes cuspidatus; cg C. gracilis; c1 Ceratozetes sp 1; dh Diapterobates humeralis; eb Eobrachychthonius borealis?; ls Liochthonius nr simplex; l1 Liochthonius sp 1; l2 Liochthonius sp 2; l5 Liochthonius sp 5; oc Oppiella clavigera; on O. nova; pa Paleacarus nr hystricinus; p1 Parisuctobelba sp 1; qq Quadroppia quadricarinata; q1 Quatrobelba sp 1; sb Suctobelba sp 1; se Synchthonius elegans; si Sellnickochthonius immaculatus; ss Sellnickochthonius suecicus; s2 Suctobelbella sp 2; s3 Suctobelbella sp 3; s4 Suctobelbella sp 4; tv Tectocepheus velatus.

8 1678 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 Fig. 5. PCA of microarthropods in the FH layer in plots 1 and 2 year after the introduction of D. octaedra n ˆ 22). Codes are as follows: WORM WT nal worm biomass; ARTH Arthropleona; AST astigmata; IMM juvenile oribatids; MESO mesostigmatids; ORIB adult oribatids; SYM Symphypleona; TARS tarsonemids. numbers and biomass of worms, the L 2 (sensu Kendrick and Burges, 1962) and FH layers were entirely replaced with casts. Changes of this magnitude to the physical structure of the soil are re ected in the negative correlation between worm biomass and (i) oribatid species richness, (ii) the abundances of 18 oribatid species, and (iii) the total abundances of adult and juvenile oribatids, astigmatids, Actinedida, mesostigmatids and Arthropleona in the FH layer, the layer of maximum worm activity. Of the 18 oribatid species negatively a ected by worm activities, most were small species, such as Brachychthoniidae (8 species) and Oppioidea (8 species) and the others were C. gracilis and Paleacarus nr hystricinus. Similarly, in other studies, small oribatids, especially those in the Brachychthoniidae, Oppiidae and Poronota, were negatively a ected by earthworm activities (Hamilton and Sillman, 1989; Maraun et al., 1999). In contrast, in the L layer, which is physically much less diverse than the FH layer, worm biomass correlated positively with oribatid species richness and diversity. Under eld conditions, the L layer is subject to desiccation and D. octaedra, like other earthworms, is very sensitive to desiccation (Lee, 1985; Edwards and Bohlen, 1996; McLean et al., 1996). Occasionally, during rainy weather, the earthworms would be able to move into this layer where their casting activities would add new substrates, increasing the microhabitat diversity (and possibly also the moisture holding capacity) of this layer, thus increasing oribatid diversity. In the L layer, several small Brachychthoniidae (L. simplex, S. immaculatus, S. suecicus ) and Q. quadricarinata, T. velatus, and Eu. marshalli were present only in the worm treatment plots at 1 and/or 2 year. While this is suggestive and tends to support this idea, in view of the small number of species and individuals in this layer it may merely re ect random occurrence. Enhancement of physical structure by earthworm activities occurred in other experiments where increased mesofaunal species diversity and abundances were

9 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671± observed. In large patches containing anecic and endogeic earthworms in pastures, larger individuals and species of Collembola were observed than in those patches without or with few earthworms (Loranger et al., 1998; Marinissen and Bok, 1988). In the Dutch pasture, earthworm activities were associated with an increase in the abundance of larger soil pores (Marinissen and Bok, 1988), which is an important component of microhabitat diversity. Loranger et al. (1998) observed higher abundance, diversity and equitability of Collembola and higher abundances of other microarthropods in high earthworm patches than in low earthworm patches. Another e ect of the activities of D. octaedra is the mixing of relatively undecomposed OM further down the pro le. The signi cant relationship between the C± N ratio and the abundance of oribatid species and mesofaunal groups in the A h and B m horizons suggests that the decompositional stage of the OM in these horizons is important to these fauna. It appears that O. nova, other Oppioidea, various Brachychthoniidae, C. cuspidatus and adult (in the A h horizon only) and juvenile oribatids, and Arthropleona all prefer less decomposed OM and therefore bene t from the mixing of OM from upper layers into this horizon. Since the Brachychthoniidae and Oppioidea are fungivorous, and the fungal assemblages on OM di er at di erent decay stages (e.g. Kendrick and Burges, 1962; Widden and Parkinson, 1973), oribatid preference for less decomposed OM probably re ects a preference for fungal species on less decomposed OM. D. humeralis apparently did not bene t from the incorporation of less decomposed OM in the A h and B m horizons. Since other members of this family are herbofungivorous grazers or herbivorous browsers (Siepel and de Ruiter-Dijkman, 1993) D. humeralis may also be able to graze on plant materials. Generally, plant material must be moist and rather decomposed before oribatids are able to graze it (Luxton, 1972), so it is not surprising that the addition of less decomposed Fig. 6. PCA of microarthropods in the A h in plots 1 and 2 year after the introduction of D. octaedra n ˆ 13). Codes are as follows: PH ph; C/ N C±N ratio; ACT Actinedida; ARTH Arthropleona; AST astigmata; IMM juvenile oribatids; MESO mesostigmatids; ORIB adult oribatids; SYM Symphypleona; TARS tarsonemids.

10 1680 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 material to these horizons was not an advantage for D. humeralis. During epigeic earthworm ingestion and gut passage, organic materials are comminuted, resulting in increased microbial respiration (Daniel and Anderson, 1992) or no e ect on respiration (Scheu and Parkinson, 1994), decreased microbial biomass (Scheu and Parkinson, 1994), higher bacterial, fungal and actinomycete densities (Daniel and Anderson, 1992; KrisÏ tuê - fek et al., 1992, 1994), and a decrease in the fungal-tobacterial ratio (Scheu and Parkinson, 1994). Although there are indications that some of the soil fauna are regulated from below (e.g. Berg et al., 1998; Klironomos and Kendrick, 1995; Scheu and Schaefer, 1998), there are few data on what aspects of the microbial community may be important to oribatid species, diversity or abundances. Do microbial biomass, fungal richness or diversity, the presence of certain species or the fungal-to-bacterial ratio in uence oribatid species, diversity and abundance? Further, do these relationships between the microbial and oribatid communities still hold under the signi cant physical alterations to the soil pro le due to earthworm activities? These important questions require further experimental investigation. Whether earthworms, such as D. octaedra are competing with or consuming oribatids or other microarthropods can not be answered by the data from the present experiment. 5. Conclusions The e ects of the activities of D. octaedra over 2 years on the oribatid community and microarthropod abundances include (i) decreased oribatid species richness in the FH layer and B m horizon, (ii) increased oribatid species richness and diversity in the L layer, (iii) decreases in the abundances of 18 oribatid species in the FH layer, (iv) decreases in the abundances of adult and juvenile oribatids, astigmatids, mesostigmatids, Actinedida and Arthropleona in the FH layer. These e ects were attributed to the changes in the physical structure of the organic layers of the soil. Acknowledgements This work was supported by an NSERC Operating Grant to D.P. and by the Biodiversity Grants Program, through the joint e orts of the sportsmen of Alberta and the Alberta Department of Environmental Protection, Fish and Wildlife Trust Fund. Our thanks to Dr. V. Behan-Pelletier for con rmation of oribatid species and to Dr. R. 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