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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 Ahand 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 Ahand 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

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

1. Introduction

There is con¯icting evidence of the eects of earth-worms 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 eects (Yeates, 1981; Hamilton and Sill-man, 1989; McLean and Parkinson, 1998; Maraun et al., 1999) have all been reported. Mechanisms which

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, 1989; Loranger et al., 1998; McLean and Parkinson, 1998; Maraun et al., 1999); (2) alteration of the chemi-cal or physichemi-cal characteristics of organic matter (OM) and its eects 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 undoubt-edly due to the diering eects of earthworms of dierent ecological strategy on soil physical structure and OM dynamics. Feeding of anecic earthworms (lar-ger litter feeding species with permanent vertical bur-rows) increases the organic matter content and porosity of mull soils, and therefore might be expected

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* Corresponding author. Louis Calder Center, Fordham Univer-sity, 53 Whippoorwill Road, Armonk, NY 10504, USA. Tel.: +1-914-273-3078 X 18; fax: +1-914-273-2167.

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to improve the physical and chemical characteristics of the soil for microarthropods. However, feeding by epi-geic 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 eects of earth-worms on soil microarthropods and the diculties of arriving at any conclusions based on soils in which earthworms have previously been active, we were for-tunate to be able to study the recent invasion of the epigeic earthworm Dendrobaena octaedra into lodge-pole 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 diameter25 cm high), the ac-tivities 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 com-pletely homogenized at the end of 6 months, we hy-pothesized that the longer term (2 years) eects 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 lodge-pole 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).

2.2. Experimental design

Five pairs of plots 1 m2 m were set up in August 1993 in a part of the lodgepole pine forest which sur-veys 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 earthwormDendrobaena octaedra

(Savigny) was added to the worm plots at numbers equivalent to its 1993 ®eld density of 250 immatures and 70 matures mÿ2, with a total biomass of 3.3 g d wt mÿ2

. 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.

2.3. 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.

2.4. Microarthropod abundances

At each of the sampling times one core 5.5 cm diam-eter was taken from each plot to assess microarthro-pod abundances. Cores were separated into L and FH layers and into Ah and Bm 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 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 Ah horizon

devel-oped in some plots but not in others, and was there-fore 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.

2.5. Statistical analysis

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en-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 pro-portion of the variation in the species data (ter Braak, 1995). Since the conditions in each soil layer/horizon were dierent, the analysis was conducted on each layer/horizon separately.

3. Results

3.1. Earthworm numbers and biomass

Earthworm numbers ranged from 0 to 3349 individ-uals mÿ2, with a mean of 854 individuals mÿ2. Earth-worm biomass ranged from 0 to 39.9 g DW mÿ2, with a mean of 8.3 g DW mÿ2.

Fig. 1. PCA of oribatid community characteristics in the L layer in plots 1 and 2 year after the introduction ofD. octaedran20). 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.

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 Ahand Bmhorizonsn20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times

L FH Ah 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)

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3.2. Eects 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 contentp<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 posi-tively with diversity and richness and negaposi-tively with dominance.

In the FH layer, ®nal worm biomassp<0:05

cor-related 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 Ah 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

vari-ation in oribatid community parameters (data not shown). Moisture content correlated positively with diversity and negatively with dominance.

In the Bm 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 com-munity parameters (data not shown). In this layer worm biomass correlated positively with oribatid dom-inance and negatively with richness, while pH corre-lated positively with richness and negatively with dominance.

3.3. Eects 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).

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In the FH layer, moisture content p<0:01

corre-lated 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, Bra-chychthonius bimaculatus and negatively correlated with Liochthonius spp 1, 2 and 4, O. clavigera,

Liochthonius nr lapponicus, L. nr simplex, Neoliochtho-nius 1, O. nova, Suctobelbella spp 1, 2, 3, 5 and 6. Final worm biomass was negatively correlated with

Sellnickochthonius immaculata,Sy. elegans,Sy. crenula-tus, Autogneta 1, C. gracilis, Parisuctobelba 1, Sucto-belba 1, Paleacarus 1, Suctobelbella 1, 2, 3 and 6,

Liochthonius 2,O. nova, Neoliochthonius 1,L. lapponi-cus,S. suecica,L.nrsimplex.

In the Ah and Bm horizons, neither the initial

treat-ment nor ®nal worm biomass correlated signi®cantly with any PCA axes. The C±N ratio p<0:05, p<

0:05correlated with the ®rst PCA axis, accounting for

97% and 78% of the variation in the oribatid species data, in the Ah and Bm horizons, respectively. In the

Ah horizon, C±N ratio correlated positively with O. nova, O. clavigera, C. cuspidatus, Dyobelba1, Suctobel-bella2 and 4,Liochthonius 2,Sy. elegans, S. immacula-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 1 and 5, L. nr simplex, L.

nr lapponicus, Eueremaeus tetrosus, S. immaculatus, B. impressus, Suctobelbella1,C. cuspidatusand correlated negatively with D. humeralis and Parisuctobelba 1 (data not shown).

3.4. Eects on microarthropod abundances

The total abundances of mites and Collembola extracted at 1 year were equivalent to 174,100 and 28,000 mÿ2, respectively. At 2 years the abundances were 134,900 and 28,800 mÿ2, respectively. Abun-dances of microarthropods were highest in the FH layer followed by the Ahhorizon (Table 3).

In the L layer C±N ratio correlated p<0:05 with Table 2

Mean (standard error) raw abundances of oribatid species in the L and FH layers and the Ahand Bmhorizonsn20, 22, 13, 17, respectively) per 5.5 cm diameter core over all plots and sampling times

L FH Ah Bm

PaleacarusnrhystricinusTraÈgaÊrdh 0 (0) 5 (10) 0 (0) 0 (0)

Liochthoniusnrlapponicus(TraÈgaÊrdh) 0 (0) 3 (5) 0 (0) 0 (0)

Liochthonius simplex(Forsslund) 0 (1) 3 (6) 1 (1) 0 (0)

Liochthoniussp 1 0 (0) 2 (3) 0 (0) 0 (0)

Liochthoniussp 2 0 (0) 12 (28) 1 (2) 1 (1)

Liochthoniussp 4 0 (0) 2 (3) 0 (1) 1 (2)

Liochthoniussp 5 0 (0) 1 (2) 0 (0) 0 (1)

Neoliochthoniussp 1 0 (0) 3 (5) 0 (1) 0 (0)

Sellnickochthonius immaculatusForsslund 0 (0) 3 (4) 0 (0) 0 (0)

Sellnickochthonius suecicusForsslund 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)

Parisuctobelbasp 1 1 (2) 29 (54) 5 (7) 2 (3)

Suctobelbasp 1 0 (0) 2 (5) 1 (1) 0 (0)

Suctobelbellasp 1 0 (0) 1 (3) 0 (1) 0 (0)

Ceratozetes gracilis(Michael) 0 (0) 7 (16) 1 (2) 0 (0)

Ceratozetessp 1 0 (1) 8 (12) 2 (3) 0 (1)

Diapterobates humeralis(Hermann) 0 (0) 5 (12) 0 (0) 1 (2)

Table 3

Mean (standard error) raw abundances of adult and juvenile oriba-tids, Actinedida, astigmaoriba-tids, mesostigmaoriba-tids, tarsonemids, Arthro-pleona, and Symphypleona in the L and FH layers and in the Ah and Bmhorizonsn20, 22, 13, 17, respectively) per 5.5 cm diam-eter core over all plots and sampling times

L FH Ah Bm

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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 tarsone-mids and negatively with the abundances of adult ori-batids, mesostigmatids and Arthropleona. Moisture content correlated positively with the abundance of adult and juvenile oribatids, mesostigmatids, Symphy-pleona and Actinedida.

In the FH layer, ®nal worm biomass correlatedp<

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 Ahand Bmhorizons, the C±N ratio correlated

p<0:05with the ®rst PCA axis, accounting for 89%

and 72% of the variation in microarthropod abun-dances, respectively. In the Ah horizon, C±N ratio

cor-related positively with the abundances of adult and juvenile oribatids, Arthropleona, astigmatids, mesostig-matids and Actinedida and negatively with Symphy-pleona (Fig. 6). In the Bm horizon, C±N ratio

correlated positively with the abundances of juvenile oribatids, tarsonemids, astigmatids, mesostigmatids, Arthropleona and Actinedida (data not shown).

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4. Discussion

Two important ways in which epigeic earthworm feeding diers from that of anecic and endogeic earth-worms are that epigeics feed mainly on relatively unde-composed litter, while anecics and endogeics feed mainly on partially decomposed and highly decom-posed 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 pas-sage results in intimate mixing of mineral and trans-formed organic materials resulting in the well-documented eects on C and N in these casts (e.g. Edwards and Bohlen, 1996). Epigeic earthworm feed-ing activities may aect 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 mi-crobial food resources, and predation.

There is evidence that oribatid species, although feeding on similar substrates, dier suciently in size to be able to exploit dierent 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 microha-bitat 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 dierentiated L and F layers and a thin (1±2 cm) H layer above a Bm horizon.

Or-ganic materials in these layers are quite distinct physi-cally and chemiphysi-cally, and provide a variety of microhabitats for microarthropods (e.g. Berg et al., 1998). In year 2, in the two plots with the highest

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numbers and biomass of worms, the L2 (sensu

Ken-drick 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 nega-tive correlation between worm biomass and (i) oribatid species richness, (ii) the abundances of 18 oribatid species, and (iii) the total abundances of adult and ju-venile oribatids, astigmatids, Actinedida, mesostigma-tids and Arthropleona in the FH layer, the layer of maximum worm activity. Of the 18 oribatid species negatively aected 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 stu-dies, small oribatids, especially those in the Bra-chychthoniidae, Oppiidae and Poronota, were negatively aected 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

corre-lated 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 ca-pacity) of this layer, thus increasing oribatid diversity. In the L layer, several small Brachychthoniidae (L. simplex,S. immaculatus,S. suecicus) and Q. quadricar-inata, 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.

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observed. In large patches containing anecic and endo-geic 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 (Marinis-sen 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 micro-arthropods in high earthworm patches than in low earthworm patches.

Another eect 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 Ah and Bmhorizons suggests

that the decompositional stage of the OM in these hor-izons is important to these fauna. It appears that O.

nova, other Oppioidea, various Brachychthoniidae, C. cuspidatus and adult (in the Ah horizon only) and

ju-venile 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 dier at dierent 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. humeralisapparently did not bene®t from the in-corporation of less decomposed OM in the Ahand Bm

horizons. Since other members of this family are her-bofungivorous 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

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material to these horizons was not an advantage for

D. humeralis.

During epigeic earthworm ingestion and gut pas-sage, organic materials are comminuted, resulting in increased microbial respiration (Daniel and Anderson, 1992) or no eect on respiration (Scheu and Parkin-son, 1994), decreased microbial biomass (Scheu and Parkinson, 1994), higher bacterial, fungal and actino-mycete densities (Daniel and Anderson, 1992; KrisÏtuÊ-fek et al., 1992, 1994), and a decrease in the fungal-to-bacterial 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; Klirono-mos 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 relation-ships between the microbial and oribatid communities still hold under the signi®cant physical alterations to the soil pro®le due to earthworm activities? These im-portant questions require further experimental investi-gation.

Whether earthworms, such as D. octaedra are com-peting with or consuming oribatids or other microar-thropods can not be answered by the data from the present experiment.

5. Conclusions

The eects of the activities of D. octaedra over 2 years on the oribatid community and microarthropod abundances include (i) decreased oribatid species rich-ness in the FH layer and Bmhorizon, (ii) increased

ori-batid 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 eects 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 Pro-gram, through the joint eorts 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. Norton for the identi®cation of oribatid juveniles, Acaridida and Endeostigmata.

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