Dendrobaena Octaedra Changes the Oribatid Community and Microarthropod Abundances in a Pine Forest

Soil Biology & Biochemistry 32 (2000) 1671±1681 www.elsevier.com/locate/soilbio

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 eects 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

Ah and Bm 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 eects were attributed to the changes in the physical structure of the organic layers of the soil. In the Ah and Bm 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 Ah 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. 7 2000 Elsevier Science Ltd. All rights reserved.

Keywords: Dendrobaena octaedra; Earthworm invasion; Oribatid community; Microarthropods

1. Introduction have been invoked to explain these eects have included: (1) alteration in the physical structure of the soil (Marinissen and Bok, 1988; Hamilton and Sillman, There is con¯icting evidence of the eects of earth- 1989; Loranger et al., 1998; McLean and Parkinson, worms on soil microarthropods (arthropods between 1998; Maraun et al., 1999); (2) alteration of the chemi- 200 mm and 2 mm, including mites and Collembola). cal or physical characteristics of organic matter (OM) Increased microarthropod abundance and diversity and its eects on the soil microbes (Yeates, 1981; (Marinissen and Bok, 1988; Loranger et al., 1998), Hamilton and Sillman, 1989; Loranger et al., 1998; decreased abundance (Dash et al., 1980; Yeates, 1981) Maraun et al., 1999); (3) competition for food (Brown, and mixed eects (Yeates, 1981; Hamilton and Sill- 1995); and (4) predation (Dash et al., 1980). Some of man, 1989; McLean and Parkinson, 1998; Maraun et the discrepancies between these studies are undoubt- al., 1999) have all been reported. Mechanisms which edly due to the diering eects of earthworms of dierent ecological strategy on soil physical structure and OM dynamics. Feeding of anecic earthworms (lar- * Corresponding author. Louis Calder Center, Fordham Univer- ger litter feeding species with permanent vertical bur- sity, 53 Whippoorwill Road, Armonk, NY 10504, USA. Tel.: +1- 914-273-3078 X 18; fax: +1-914-273-2167. rows) increases the organic matter content and E-mail address: [email protected] (M.A. McLean). porosity of mull soils, and therefore might be expected

0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved. PII: S0038-0717(00)00083-3 1672 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 to improve the physical and chemical characteristics of of the forest where earthworms had already been the soil for microarthropods. However, feeding by epi- established for a few years. geic earthworms (smaller litter feeding species con®ned In September 1994 and September 1995 the plots to the organic and upper mineral layers) mixes mineral were sampled for microarthropod abundances and for material into the organic layers, and might be expected assessment of worm abundance and biomass. to reduce physical and chemical soil qualities for microarthropods in the organic layers of the soil. 2.3. Earthworm abundance and biomass Given the paucity of data on the eects of earthworms on soil microarthropods and the diculties of At each sampling time one core 10.5 cm diameter arriving at any conclusions based on soils in which was taken from each plot and the earthworms present earthworms have previously been active, we were for- were heat extracted (Kempson et al., 1963) and tunate to be able to study the recent invasion of the counted as small (<10 mm long) immature, large epigeic earthworm Dendrobaena octaedra into lodge- immature, mature and aclitellate adults. Oven dry pole pine forest in SW Alberta, Canada. We used two weights of each of the worm size classes were used to approaches: short-term (6 months) laboratory studies obtain estimates of worm biomass at each of the (McLean and Parkinson, 1997a, 1998), and longer sampling times. Mean biomass of a mature worm was term (2 years) ®eld studies (McLean and Parkinson, 27 mg DW. 1997b, 2000, the present study). Under conditions of optimum moisture and temperature in mesocosms 2.4. Microarthropod abundances (intact soil cores 30 cm diameter Â 25 cm high), the activities of D. octaedra increased oribatid diversity and At each of the sampling times one core 5.5 cm diam- abundances (McLean and Parkinson, 1998). This was eter was taken from each plot to assess microarthro- attributed to an increase in spatial heterogeneity pod abundances. Cores were separated into L and FH through the addition of casts to the organic materials layers and into Ah and Bm horizons where possible already present. However, since organic layers in the and the microarthropods were heat extracted using a mesocosms with the highest worm numbers were com- high gradient extractor (Merchant and Crossley, 1970) pletely homogenized at the end of 6 months, we hy- from each layer and horizon. Microarthropods were pothesized that the longer term (2 years) eects of D. preserved in 70% ethanol and identi®ed: adult oribatid octaedra would be decreased oribatid diversity and to species where possible; juvenile oribatids to genus microarthropod abundance. where possible; other mites and Collembola to subor- der. Due to the heterogeneity of the soil and the pre-

sence of rocks, some samples did not include the Bm horizon. Due to worm activities, an A horizon devel- 2. Materials and methods h oped in some plots but not in others, and was therefore not sampled in all cases. 2.1. Site description Oribatid community parameters (species richness (S ), dominance (d ), diversity (1/D )) were calculated The site of this experiment was a 90-year old lodge- from the abundance data for all horizons in all plots. pole pine (Pinus contorta var. latifolia Engelm.) forest in the Kananaskis Valley of SW Alberta, Canada. For 2.5. Statistical analysis a more detailed description see McLean and Parkinson (1997b). At the time the plots were set up, earthworms were already invading the forest and therefore some of the 2.2. Experimental design ``control'' plots contained earthworms (McLean and Parkinson, 1997b) so ®nal earthworm biomass was Five pairs of plots 1 m Â 2 m were set up in August included in the analysis. Data were analyzed using 1993 in a part of the lodgepole pine forest which sur- ordination which allows the simultaneous analysis of veys had shown to be free from earthworms. Within the whole community. Principal Components Analysis each pair of plots, two treatments (control without (PCA), a linear and indirect ordination method was earthworms and treatment with worms) were randomly chosen since (i) the range of sample scores was low, assigned. The epigeic earthworm Dendrobaena octaedra making a linear method preferable to a unimodal (Savigny) was added to the worm plots at numbers method, (ii) indirect ordination methods allow the dis- equivalent to its 1993 ®eld density of 250 immatures covery of the largest variation in the species data with- and 70 matures m2, with a total biomass of 3.3 g d out being constrained by possibly irrelevant wt m2. The earthworms used were heat extracted environmental variables, and (iii) analysis can be fol- (Kempson et al., 1963) from pine forest ¯oor in a part lowed by correlation of the extracted axes with en- M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 1673

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 Ah and Bm horizons n 20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times

LFHAh Bm

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 3. Results supplied environmental variables (in this case, ®nal worm biomass, organic matter content (OM), moisture 3.1. Earthworm numbers and biomass content, pH, C±N ratio) account for a signi®cant pro- portion of the variation in the species data (ter Braak, Earthworm numbers ranged from 0 to 3349 individ- 1995). Since the conditions in each soil layer/horizon uals m2, with a mean of 854 individuals m2. Earth- were dierent, the analysis was conducted on each worm biomass ranged from 0 to 39.9 g DW m2, with layer/horizon separately. a mean of 8.3 g DW m2.

Fig. 1. PCA of oribatid community characteristics in the L layer in plots 1 and 2 year after the introduction of D. octaedra n 20). Codes are as follows; WORM WT ®nal worm biomass; H2O moisture content; BP Berger-Parker Index of Dominance; RICH species richness; IS Inverse Simpson Index of Diversity. 1674 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681

3.2. Eects on oribatid community structure ation in oribatid community parameters (data not shown). Moisture content correlated positively with Number of individuals, species richness and diversity diversity and negatively with dominance. were highest and dominance was lowest in the FH In the Bm horizon, ®nal worm biomass p < 0:05 layer (Table 1). and pH p < 0:05 correlated with the ®rst PCA axis, In the L layer, moisture content p < 0:01 and ®nal accounting for 63% of the variation in oribatid com- worm biomass p < 0:05 correlated with the ®rst PCA munity parameters (data not shown). In this layer axis, accounting for 99% of the variation in oribatid worm biomass correlated positively with oribatid dom- community parameters (Fig. 1). In this layer both inance and negatively with richness, while pH corre- moisture content and worm biomass correlated posi- lated positively with richness and negatively with tively with diversity and richness and negatively with dominance. dominance. In the FH layer, ®nal worm biomass p < 0:05 cor- 3.3. Eects on oribatid species abundances related with the ®rst PCA axis, accounting for 83% of the variation in oribatid community parameters In the course of this investigation, 55 oribatid (Fig. 2). In this layer ®nal worm biomass correlated species were extracted from the plots, many of which negatively with richness. were observed only once. Mean abundances of the 20

In the Ah horizon, neither initial treatment nor ®nal most common species are listed in Table 2. worm biomass correlated with the extracted PCA axes, In the L layer, none of the supplied environmental however moisture content correlated p < 0:05 with variables correlated with any of the PCA axes (data the second PCA axis, accounting for 19% of the vari- 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 22). Codes are as follows; WORM WT ®nal worm biomass; BP Berger-Parker Index of Dominance; RICH species richness; IS Inverse Simpson Index of Diver- sity. M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 1675

Table 2

Mean (standard error) raw abundances of oribatid species in the L and FH layers and the Ah and Bm horizons n 20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times

LFHAh Bm

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 corre- Sellnickochthonius immaculata, Sy. elegans, Sy. crenula- lated with the ®rst PCA axis and ®nal worm biomass tus, Autogneta 1, C. gracilis, Parisuctobelba 1, Sucto- p < 0:05 correlated with the second PCA axis, belba 1, Paleacarus 1, Suctobelbella 1, 2, 3 and 6, accounting for 56% and 28% of the variation in the Liochthonius 2, O. nova, Neoliochthonius 1, L. lapponi- oribatid species data, respectively (Fig. 3). Moisture cus, S. suecica, L. nr simplex. content was positively correlated with Tectocepheus In the Ah and Bm horizons, neither the initial treat- velatus, Diapterobates humeralis, Belba 2, Ceratozetes ment nor ®nal worm biomass correlated signi®cantly 1, Paleacarus 1, Trhypochthonius tectorum, Suctobelba with any PCA axes. The C±N ratio p < 0:05, p < 1, Ceratozetes gracilis, Parisuctobelba 1, Autogneta 1, 0:05 correlated with the ®rst PCA axis, accounting for Synchthonius crenulatus, Sy. elegans, Dyobelba 1, Bra- 97% and 78% of the variation in the oribatid species chychthonius bimaculatus and negatively correlated data, in the Ah and Bm horizons, respectively. In the with Liochthonius spp 1, 2 and 4, O. clavigera, Ah horizon, C±N ratio correlated positively with O. Liochthonius nr lapponicus, L. nr simplex, Neoliochtho- nova, O. clavigera, C. cuspidatus, Dyobelba 1, Suctobel- nius 1, O. nova, Suctobelbella spp 1, 2, 3, 5 and 6. bella 2and4,Liochthonius 2, Sy. elegans, S. immacula- Final worm biomass was negatively correlated with tus, Q. quadricarinata and negatively with D. humeralis, Paleacarus 1, and Suctobelba 1 (Fig. 4). In

the Bm horizon, the C±N ratio correlated positively with O. nova, Liochthonius 1and5,L. nr simplex, L. Table 3 nr lapponicus, Eueremaeus tetrosus, S. immaculatus, B. Mean (standard error) raw abundances of adult and juvenile oribatids, Actinedida, astigmatids, mesostigmatids, tarsonemids, Arthro- impressus, Suctobelbella 1, C. cuspidatus and correlated pleona, and Symphypleona in the L and FH layers and in the Ah negatively with D. humeralis and Parisuctobelba 1 and Bm horizons n 20, 22, 13, 17, respectively) per 5.5 cm diam- (data not shown). eter core over all plots and sampling times

LFHAh Bm 3.4. Eects on microarthropod abundances

Juvenile oribatids 4 (4) 31 (33) 17 (22) 6 (8) Adult oribatids 2 (3) 148 (129) 55 (57) 20 (17) The total abundances of mites and Collembola Actinedida 2 (2) 21 (19) 13 (10) 6 (5) extracted at 1 year were equivalent to 174,100 and Astigmatids 0 (0) 21 (34) 3 (8) 3 (4) 28,000 m2, respectively. At 2 years the abundances Mesostigmatids 1 (1) 32 (21) 7 (5) 3 (4) were 134,900 and 28,800 m2, respectively. Abun- Tarsonemids 4 (7) 9 (10) 1 (1) 0 (1) dances of microarthropods were highest in the FH Arthropleona 1 (2) 41 (31) 15 (8) 7 (7) Symphypleona 0 (0) 1 (1) 0 (0) 0 (0) layer followed by the Ah horizon (Table 3). In the L layer C±N ratio correlated p < 0:05 with 1676 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 the ®rst PCA axis and moisture content correlated abundances of Symphypleona and negatively with the p < 0:05 with the second PCA axis, accounting for abundances of adult and juvenile oribatids, Actinedida, 65% and 16% of the variation in the microarthropod astigmatids, mesostigmatids and Arthropleona. abundances, respectively (data not shown). C±N ratio In the Ah and Bm horizons, the C±N ratio correlated correlated positively with the abundance of tarsone- p < 0:05 with the ®rst PCA axis, accounting for 89% mids and negatively with the abundances of adult ori- and 72% of the variation in microarthropod abun- batids, mesostigmatids and Arthropleona. Moisture dances, respectively. In the Ah horizon, C±N ratio cor- content correlated positively with the abundance of related positively with the abundances of adult and adult and juvenile oribatids, mesostigmatids, Symphy- juvenile oribatids, Arthropleona, astigmatids, mesostig- pleona and Actinedida. matids and Actinedida and negatively with Symphy-

In the FH layer, ®nal worm biomass correlated p < pleona (Fig. 6). In the Bm horizon, C±N ratio 0:05 with the ®rst PCA axis, accounting for 88% of correlated positively with the abundances of juvenile the variation in microarthropod abundances (Fig. 5). oribatids, tarsonemids, astigmatids, mesostigmatids, Final worm biomass correlated positively with the 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 22). Codes as follows: H2O moisture content; WORM WT ®nal worm biomass; a1 Autogneta sp 1; bb Brachychthonius bimaculatus;biBrachychthonius impressus;ccCeratozetes cuspidatus;cgC. gracilis;c1Ceratozetes sp 1; dh Diapterobates humeralis and Belba sp 2; dr Dentizetes rudentiger;eaEremaeus translamellatus; eb Eobrachychthonius borealis?; el Epidamaeus longitarsalis;emEueremaeus marshalli;erEupterotegaeus rostratus;esEueremaeus sp 1; et Euere- maeus tetrosus;e1Epidamaeus sp 1; e3 Epidamaeus sp 3; ll Liochthonius nr lapponicus;l1Liochthonius 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;n1Neoliochthonius sp 1; on O. nova;paPaleacarus nr hystricinus;p1Parisuctobelba sp 1; qq Quadroppia quadricarinata;q1Quatrobelba sp 1; sb Suctobelba sp 1; sc Synchthonius crenulatus;seSynchthonius elegans;siSellnickochthonius immaculatus;s1Suctobelbella sp 1; s2 Suctobelbella sp 2 and Oppiella clavigera;s3Suctobelbella sp 3; s4 Suctobelbella sp 4; tt Trhypochthonius tectorum;tvTectocepheus velatus;t1Tectocepheus sp 1. M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 1677

4. Discussion layers, through the impacts of comminution on their microbial food sources, or through competition for mi- Two important ways in which epigeic earthworm crobial food resources, and predation. feeding diers from that of anecic and endogeic earth- There is evidence that oribatid species, although worms are that epigeics feed mainly on relatively unde- feeding on similar substrates, dier suciently in size composed litter, while anecics and endogeics feed to be able to exploit dierent sized pores in organic mainly on partially decomposed and highly decom- soil layers, and therefore may be spatially separated posed organic materials, respectively (Daniel and (Anderson, 1978; Walter and Norton, 1984). In a Anderson, 1992; Edwards and Bohlen, 1996), and that detailed analysis of the relationship between microha- epigeic gut passage results in comminuted but not bitat diversity and oribatid diversity, Anderson (1978) transformed organic materials (Ponge, 1991; Daniel observed strong correlations between oribatid diversity and Anderson, 1992; Ziegler and Zech, 1992; Edwards and inter- and intra-habitat diversity. In our study, and Bohlen, 1996), while endogeic and anecic gut pas- prior to earthworm invasion, the lodgepole pine forest sage results in intimate mixing of mineral and trans- ¯oor consisted of well dierentiated L and F layers formed organic materials resulting in the well- and a thin (1±2 cm) H layer above a Bm horizon. Or- documented eects on C and N in these casts (e.g. ganic materials in these layers are quite distinct physi- Edwards and Bohlen, 1996). Epigeic earthworm feed- cally and chemically, and provide a variety of ing activities may aect the soil microarthropods microhabitats for microarthropods (e.g. Berg et al., through changes in the structure of the soil organic 1998). In year 2, in the two plots with the highest

Fig. 4. PCA of oribatid species in the Ah horizon in plots 1 and 2 year after the introduction of D. octaedra n 13). Codes as follows: C/N C± N ratio; cc Ceratozetes cuspidatus;cgC. gracilis;c1Ceratozetes sp 1; dh Diapterobates humeralis;ebEobrachychthonius borealis?; ls Liochthonius nr simplex;l1Liochthonius sp 1; l2 Liochthonius sp 2; l5 Liochthonius sp 5; oc Oppiella clavigera;onO. nova;paPaleacarus nr hystricinus;p1Par- isuctobelba sp 1; qq Quadroppia quadricarinata;q1Quatrobelba sp 1; sb Suctobelba sp 1; se Synchthonius elegans;siSellnickochthonius immaculatus;ssSellnickochthonius suecicus;s2Suctobelbella sp 2; s3 Suctobelbella sp 3; s4 Suctobelbella sp 4; tv Tectocepheus velatus. 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 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 L2 (sensu Ken- lated positively with oribatid species richness and drick and Burges, 1962) and FH layers were entirely diversity. Under ®eld conditions, the L layer is subject replaced with casts. Changes of this magnitude to the to desiccation and D. octaedra, like other earthworms, physical structure of the soil are re¯ected in the nega- is very sensitive to desiccation (Lee, 1985; Edwards tive correlation between worm biomass and (i) oribatid and Bohlen, 1996; McLean et al., 1996). Occasionally, species richness, (ii) the abundances of 18 oribatid during rainy weather, the earthworms would be able species, and (iii) the total abundances of adult and ju- to move into this layer where their casting activities venile oribatids, astigmatids, Actinedida, mesostigma- would add new substrates, increasing the microhabitat tids and Arthropleona in the FH layer, the layer of diversity (and possibly also the moisture holding ca- maximum worm activity. Of the 18 oribatid species pacity) of this layer, thus increasing oribatid diversity. negatively aected by worm activities, most were small In the L layer, several small Brachychthoniidae (L. species, such as Brachychthoniidae (8 species) and simplex, S. immaculatus, S. suecicus ) and Q. quadricar- Oppioidea (8 species) and the others were C. gracilis inata, T. velatus, and Eu. marshalli were present only and Paleacarus nr hystricinus. Similarly, in other stu- in the worm treatment plots at 1 and/or 2 year. While dies, small oribatids, especially those in the Bra- this is suggestive and tends to support this idea, in chychthoniidae, Oppiidae and Poronota, were view of the small number of species and individuals in negatively aected by earthworm activities (Hamilton this layer it may merely re¯ect random occurrence. and Sillman, 1989; Maraun et al., 1999). Enhancement of physical structure by earthworm ac- In contrast, in the L layer, which is physically much tivities occurred in other experiments where increased less diverse than the FH layer, worm biomass corre- mesofaunal species diversity and abundances were M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 1679 observed. In large patches containing anecic and endo- nova, other Oppioidea, various Brachychthoniidae, C. geic earthworms in pastures, larger individuals and cuspidatus and adult (in the Ah horizon only) and ju- species of Collembola were observed than in those venile oribatids, and Arthropleona all prefer less patches without or with few earthworms (Loranger et decomposed OM and therefore bene®t from the mixing al., 1998; Marinissen and Bok, 1988). In the Dutch of OM from upper layers into this horizon. Since the pasture, earthworm activities were associated with an Brachychthoniidae and Oppioidea are fungivorous, increase in the abundance of larger soil pores (Marinis- and the fungal assemblages on OM dier at dierent sen and Bok, 1988), which is an important component decay stages (e.g. Kendrick and Burges, 1962; Widden of microhabitat diversity. Loranger et al. (1998) and Parkinson, 1973), oribatid preference for less observed higher abundance, diversity and equitability decomposed OM probably re¯ects a preference for of Collembola and higher abundances of other microfungal species on less decomposed OM. arthropods in high earthworm patches than in low D. humeralis apparently did not bene®t from the in- earthworm patches. corporation of less decomposed OM in the Ah and Bm Another eect of the activities of D. octaedra is the horizons. Since other members of this family are her- mixing of relatively undecomposed OM further down bofungivorous grazers or herbivorous browsers (Siepel the pro®le. The signi®cant relationship between the C± and de Ruiter-Dijkman, 1993) D. humeralis may also N ratio and the abundance of oribatid species and be able to graze on plant materials. Generally, plant mesofaunal groups in the Ah and Bm horizons suggests material must be moist and rather decomposed before that the decompositional stage of the OM in these hor- oribatids are able to graze it (Luxton, 1972), so it is izons is important to these fauna. It appears that O. not surprising that the addition of less decomposed

Fig. 6. PCA of microarthropods in the Ah in plots 1 and 2 year after the introduction of D. octaedra n 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. 1680 M.A. McLean, D. Parkinson / Soil Biology & Biochemistry 32 (2000) 1671±1681 material to these horizons was not an advantage for References D. humeralis. During epigeic earthworm ingestion and gut pas- Anderson, J.M., 1978. Inter- and intra-habitat relationships between sage, organic materials are comminuted, resulting in woodland cryptostigmata species diversity and the diversity of increased microbial respiration (Daniel and Anderson, soil and litter habitats. Oecologia 32, 341±348. 1992) or no eect on respiration (Scheu and Parkin- Berg, M.P., Kniese, J.P., Bedaux, J.J.M., Verhoef, H.A., 1998. son, 1994), decreased microbial biomass (Scheu and Dynamics and strati®cation of functional groups of micro- and meso-arthropods in the organic layer of a Scots pine forest. Parkinson, 1994), higher bacterial, fungal and actino- Biology and Fertility of Soils 26, 268±284. mycete densities (Daniel and Anderson, 1992; KrisÏ tuÊ- Brown, G.G., 1995. How do earthworms aect micro¯oral and fau- fek et al., 1992, 1994), and a decrease in the fungal-to- nal community diversity? Plant and Soil 170, 209±231. bacterial ratio (Scheu and Parkinson, 1994). Although Daniel, O., Anderson, J.M., 1992. Microbial biomass and activity in there are indications that some of the soil fauna are contrasting soil materials after passage through the gut of the regulated from below (e.g. Berg et al., 1998; Klirono- earthworm Lumbricus rubellus Homeister. Soil Biology & Biochemistry 24, 465±470. mos and Kendrick, 1995; Scheu and Schaefer, 1998), Dash, M.C., Senapati, B.K., Mishra, C.C., 1980. Nematode feeding there are few data on what aspects of the microbial by tropical earthworms. Oikos 34, 322±325. community may be important to oribatid species, Edwards, C.A., Bohlen, P.J., 1996. In: Biology and Ecology of diversity or abundances. Do microbial biomass, fungal Earthworms. Chapman & Hall, London. richness or diversity, the presence of certain species or Hamilton, W.E., Sillman, D.Y., 1989. In¯uence of earthworm mid- the fungal-to-bacterial ratio in¯uence oribatid species, dens on the distribution of soil microarthropods. Biology and Fertility of Soils 8, 279±284. diversity and abundance? Further, do these relation- Kempson, D., Lloyd, M., Ghelardi, R., 1963. A new extractor for ships between the microbial and oribatid communities woodland litter. Pedobiologia 3, 1±21. still hold under the signi®cant physical alterations to Kendrick, W.B., Burges, A., 1962. Biological aspects of the decay of the soil pro®le due to earthworm activities? These im- Pinus sylvestris leaf litter. Nova Hedwigia IV, 313±358. portant questions require further experimental investi- Klironomos, J.N., Kendrick, W.B., 1995. Relationships among gation. microarthropods, fungi and their environment. Plant and Soil 170, 183±197. Whether earthworms, such as D. octaedra are com- KrisÏ tuÊ fek, V., Ravasz, K., PizÏl, V., 1992. Changes in densities of bac- peting with or consuming oribatids or other microar- teria and microfungi during gut transit in Lumbricus rubellus and thropods can not be answered by the data from the Aporrectodea caliginosa (Oligochaeta: Lumbricidae). Soil Biology present experiment. & Biochemistry 24, 1499±1500. KrisÏ tuÊ fek, V., TajovskyÂ , K., PizÏl, V., 1994. Ultrastructural analysis of the intestinal content of earthworm Lumbricus rubellus Hom. (Annelida, Lumbricidae). Acta Microbiologica et Immunologica 5. Conclusions Hungarica 41, 283±290. Lee, K., 1985. Earthworms: Their Ecology, and Relationships with The eects of the activities of D. octaedra over 2 Soils and Land Use. Academic Press, NY. years on the oribatid community and microarthropod Loranger, G., Ponge, J.F., Blanchart, E., Lavelle, P., 1998. Impact abundances include (i) decreased oribatid species rich- of earthworms on the diversity of microarthropods in a vertisol (Martinique). Biology and Fertility of Soils 27, 21±26. ness in the FH layer and Bm horizon, (ii) increased ori- Luxton, M., 1972. Studies on the oribatid mites of a Danish beech batid species richness and diversity in the L layer, (iii) wood soil. I. Nutritional biology. Pedobiologia 12, 434±463. decreases in the abundances of 18 oribatid species in Maraun, M., Alphei, J., Bonkowski, M., Buryn, R., Migge, S., Peter, the FH layer, (iv) decreases in the abundances of adult M., Schaefer, M., Scheu, S., 1999. Middens of the earthworm and juvenile oribatids, astigmatids, mesostigmatids, Lumbricus terrestris (Lumbricidae): microhabitats for micro- and Actinedida and Arthropleona in the FH layer. These meso-fauna in forest soil. Pedobiologia 43, 276±287. Marinissen, J.C.Y., Bok, J., 1988. Earthworm-amended soil struc- eects were attributed to the changes in the physical ture: its in¯uence on Collembola populations in grassland. structure of the organic layers of the soil. Pedobiologia 32, 243±252. McLean, M.A., Parkinson, D., 1997a. Changes in structure, organic matter and microbial activity in pine forest soil following the Acknowledgements introduction of Dendrobaena octaedra (Oligochaeta: Lumbricidae). Soil Biology & Biochemistry 29, 537±540. McLean, M.A., Parkinson, D., 1997b. Soil impacts of the epigeic This work was supported by an NSERC Operating earthworm Dendrobaena octaedra on organic matter and mi- Grant to D.P. and by the Biodiversity Grants Pro- crobial activity in lodgepole pine forest. Canadian Journal of gram, through the joint eorts of the sportsmen of Forest Research 27, 1907±1913. Alberta and the Alberta Department of Environmental McLean, M.A., Parkinson, D., 1998. Impacts of the epigeic earth- Protection, Fish and Wildlife Trust Fund. Our thanks worm Dendrobaena octaedra on oribatid community diversity and microarthropod abundances in pine forest ¯oor: a mesocosm to Dr. V. Behan-Pelletier for con®rmation of oribatid study. Applied Soil Ecology 7, 125±136. species and to Dr. R. Norton for the identi®cation of McLean, M.A., Parkinson, D., 2000. Field evidence of the eects of oribatid juveniles, Acaridida and Endeostigmata. the epigeic earthworm Dendrobaena octaedra on the microfungal M.A. McLean, D. 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