OIKOS 112: 513
/524, 2006

The response of decomposers (earthworms, springtails and

microorganisms) to variations in species and functional group
diversity of plants

Alexandru Milcu, Stephan Partsch, Reinhardt Langel and Stefan Scheu

Milcu, A., Partsch, S., Langel, R. and Scheu, S. 2006. The response of decomposers
(earthworms, springtails and microorganisms) to variations in species and functional
group diversity of plants.
/ Oikos 112: 513
/524.

The responses of three decomposer groups (earthworms, springtails and

microorganisms) to manipulations in plant species diversity (1, 2, 4, 8), plant
functional group diversity (1, 2, 3, 4) and functional group identity (grasses,
legumes, small herbs, tall herbs) were studied in a microcosm experiment. Separate
and combined treatments with earthworms and springtails were set up. Two earthworm
species representing major functional groups of earthworms in grasslands were
investigated, the endogeic species Aporrectodea caliginosa (Savigny) and the anecic
species Lumbricus terrestris L. For springtails three species were investigated, the
hemiedaphic species Heteromurus nitidus (Leleup), Folsomia candida (Willem) and the
euedaphic species Protaphorura fimata (Gisin). Plant species and functional group
diversity beneficially affected A. caliginosa (increase in body weight and incorporation
of 15N from labelled litter) and P. fimata (density), presumably by changing the quality
of belowground resources. In contrast, the biomass of L. terrestris decreased with plant
species diversity but only in presence of legumes. For H. nitidus and F. candida the
identity of plant functional groups was more important than plant species diversity per
se. Also, the response of F. candida depended on earthworms. Microbial respiration
was reduced by earthworms in more diverse plant communities, which correlated with
root biomass. In contrast, microbial biomass was not affected by plant species diversity.
The results suggest that belowground resource inputs from plant roots strongly modify
decomposer performance and that the quality of the resources that enter the
belowground subsystem is more important than their quantity. The responses of
decomposers generally were not correlated with below- or aboveground plant
productivity. In addition, the results document that effects of plant community
composition on the performance of decomposer species depend on the presence of
other decomposers.

A. Milcu, S. Partsch and S. Scheu, Institut für Zoologie, Technische Universität

Darmstadt, Schnittspahnstr. 3, DE-64287 Darmstadt, Germany (amilcu@bio.tu-
darmstadt.de).
/ R Langel, Forschungszentrum Waldökosysteme, Kompetenzzentrum
Stabile Isotope, Büsgenweg. 2, DE- 37077 Göttingen, Germany.

Decomposers are crucial for transforming complex available for producers to rebuild complex organic
organic materials into inorganic forms without which matter. Despite the fact that decomposer microorgan-
dead organic material would accumulate irreversibly isms also immobilize inorganic nutrients which may
(Schlesinger 1997). The inextricable decomposer
/ result in competition with producers, the two compart-
producer co-dependency constitutes of the mineraliza- ments essentially complement each other (Harte and
tion of organic matter by decomposers making nutrients Kinzig 1993).

Accepted 27 July 2005

Copyright # OIKOS 2006
ISSN 0030-1299

OIKOS 112:3 (2006) 513

 In attempts of linking below- and aboveground cosms these hypothesis were evaluated under controlled
communities the feedback of plant communities to the conditions and well defined manipulations of the decom-
decomposer food web is often neglected. The quantity poser community. The use of 15N labelled litter allowed
and quality of resources produced by plant communities to track nutrient fluxes from dead organic matter into
strongly influence the structure of soil food webs and plants and animals.
their functioning (Wardle 2002, Scheu et al. 2003, De
Deyn et al. 2004). Plant species effects manifests not only
through the amount of litter returned to the soil (Wardle
Material and methods
et al. 1995, Groffman et al. 1996) but also through the
amount of soluble carbon compounds liberated via Experimental set-up
root exudates (Bais et al. 2004, Li et al. 2004), root
and leaf chemical composition (Satchell 1967, Hendrik- The experiment was set up in microcosms consisting of
PVC tubes (inner ¥ 10 cm, height 25 cm) which were
sen 1990, Tian et al. 1993) and the extent to which they
sealed at the bottom with 40 mm mesh. The microcosms
deplete nutrients in the soil (Grime 1994, Fransen et al.
were filled with 1.4 kg of sieved (4 mm) soil (water
1999).
content 13%). The soil (Eutric Fluvisoil, FAO Unesco
Earthworms and springtails are key decomposers
(1997); pH 8.1, carbon content 4.6%, C/N ratio 15.7,
affecting plant performance (Scheu et al. 1999, Wurst
sand content 15%, water content 13%) was taken from
et al. 2003). Earthworms as soil macrofauna decom-
the northeast corner of the Jena Biodiversity Experiment
posers modify the physical structure of the soil (Lee and
field site (Thuringia, Germany; cf. Roscher et al. 2004).
Foster 1991, Lavelle et al. 1997), alter soil microbial
Prior to use the soil was defaunated by freezing at
community composition and functioning (Brown 1995,
/228C for 14 d. Defaunation by freezing effectively kills
Scheu 2002), increase nutrient cycling (Parmelee et al.
meso- and macrofauna, whereas microfauna (nematoda,
1989, Edwards and Bohlen 1996) and affect plant growth
protozoa) in large survive (Huhta et al. 1989). A layer of
and vegetation development (Thompson et al. 1993, 15
N labeled roots of Lolium perenne (250 mg, 30 atom%
Schmidt and Curry 1999, Zaller and Arnone 1999, Scheu 15
N; fragmented B/1 mm) was placed 2 cm below the soil
2003). Springtails are important microbial grazers which surface. After placing in the microcosms the soil was
affect the structure and functioning of the microbial irrigated by adding two 50-ml portions of deionized
community in the rizosphere and plant nutrient avail- water every second day for 8 d to leach nutrients released
ability (Rusek 1998, Gange 2000). Soil microorganisms as a result of the defaunation procedure. Subsequently,
compete with plants for nutrients (Kaye and Hart 1997, microcosms were kept moist for another 14 d by adding
Hodge et al. 2000) and it has been documented that 50 ml deionized water every third day; weeds germinat-
interactions between soil microorganisms and soil in- ing during this period were removed.
vertebrates significantly affect plant performance (Bon- Plant species were selected from a species pool
kowski and Scheu 2004). However, little is known how representing central European Arrhenatherion grass-
decomposers respond to differences in plant species and lands. A total of 43 plant species were used, grown
functional group diversity. The studies that investigated from seeds in the defaunated soil and transplanted into
the effect of plant species diversity on the soil decom- the microcosms when the plants had grown to a height of
poser communities showed positive (Zaller and Arnone 2
/6 cm. Eight plant individuals consisting of four
1999, Spehn et al. 2000, Stephan et al. 2000) or no functional groups (grasses, legumes, small herbs, tall
consistent effects (Wardle et al. 1999, Gastine et al. 2003, herbs) were transplanted into each microcosm in differ-
Hedlund et al. 2003, Salamon et al. 2004). ent combinations following the design of the Jena
In this study we established a microcosm experiment Biodiversity Experiment (Roscher et al. 2004). Plant
to investigate the response of different functional groups functional groups were assessed using three groups of
of decomposers to variations in plant species and plant attributes: (1) above- and below ground morphological
functional group diversity. We expected changes in plant traits (2) phenological traits and (3) the ability for N2
biomass, root exudation and microbial community fixation. The seventeen variables created from the
composition caused by reductions in plant diversity to selected species attributes were analysed by a multi-
strongly affect the structure of the decomposer commu- variate cluster method (Ward’s method, Euclidian dis-
nity and interactions between decomposer functional tance; Kaufman and Rousseeuw 1990) in order to
groups. Specifically we hypothesized that (1) an increase identify species functional groups (Roscher et al. 2004).
in plant species and functional group diversity benefi- Monocultures and species mixtures were established
cially affect decomposer performance, (2) decomposer forming a plant species and functional group diversity
performance varies with functional group and plant gradient as given in Table 1. A total of 64 different plant
species identity, and (3) interactions between soil macro- species mixtures were set up.
fauna decomposers and fungal grazing soil invertebrates Two grams of litter material consisting mainly of grass
depend on plant community composition. Using micro- leaves was placed on top of the soil subsequently to the

514 OIKOS 112:3 (2006)

Table 1. Scheme of the 64 plant species mixtures set up in the experiment varying in species identity, number of species and
composition of functional groups (grasses (G), small herbs (Sh), tall herbs (Th) and legumes (L)). Four animal treatments were set
up per plant species mixture (control without animals, with earthworms, with Collembola, with earthworms and Collembola). (G):
Ao/Anthoxantum odoratum L., Ap/Alopecurus pratensis L., Be/Bromus erectus HUDS., Bh/Bromus hordeaceus L., Cc/
Cynosurus cristatus L., Dg /Dactylis glomerata L., Fp/Festuca pratensis HUDS., Fr/Festuca rubra L., Hl /Holcus lanatus L.,
PHp/Phleum pratense L., Pp/Poa pratensis L., Pt/Poa trivialis L., Tf/Trisetum flavescens. (Sh): Bp/Bellis perennis L., Gh/
Glechoma hederacea L., La/Leontodon autumnalis L. Lh/Leontodon hispidus L., Pl/Plantago lancelolata L., Pm/Plantago
media L., Pv/Prunella vulgaris L., To/Taraxacum officinale WEBER, Vc /Veronica chamaedrys L. (Th): Am /Achillea
millefolium L., Cb/Crepis benis L., Cj/Centaurea jacea L., Co/Cirsium oleraceum L., Cp/Cardamine pratensis L., Dc/
Daucus carota L., Ga /Galium mollugo L., Ka/Knautia arvensis L., Lv /Leucanthemum vulgare Lam., Ra/Rumex acetosa L.,
TRp/Tragopogon pratensis L. (L): Lp/Lathyrus pratensis L., Lc/Lotus corniculatus L., Ml/Medicago lupulina L., Ms/
Medicago x varia MARTYN, Ov/Onobrychis viciifolia SCOP., Td/Trifolium dubium SIBTH., Th/Trifolium hybridum L., Tr/
Trifolium repens L., Tp/Trifolium pratense L., VIc/Vicia cracca L.

Species Species Functional group Functional group Species

mixture diversity diversity composition

1
/16 1 1 4 G, 4 Sh, 4 Th, 4 L monoculture of Cc; Fp; Fr; Pp; Pl; Bp;
Pv; Gh; Co; Dc; Cb; Gm; Lp; Vic; Ov;
Ms
17
/18 2 1 2G Fp, Dg; Fr, Tf
19
/20 2 1 2 Sh Bp, To; Pl, Bp
21
/22 2 1 2 Th Cb, Dc; Cj, Ra
23
/24 2 1 2L Ov, Tr; Lc, Tp
25 2 2 GSh Tf, To
26 2 2 GSh Pp, Pl
27 2 2 ThL Cj, Td
28 2 2 ThL Dc, Ms
29 2 2 GTh Fp, Cj
30 2 2 GTh Ap, Dc
31 2 2 ShL La, Tr
32 2 2 ShL Pl, Td
33 4 1 G Ap, Pt, Ao, Be
34 4 1 Sh Pv, Pm, Pl, Lh
35 4 1 Th Am, Dc, Cp, Ka
36 4 1 L Lc, Ov, Ms, Tr
37 4 2 GSh Pt, Be, Pl, Pv
38 4 2 ThL Cp, Cb, Tr, VIc
39 4 2 GTh Fp, Pt, Am, Cb
40 4 2 ShL To, Pl, Tr, Lp
41 4 3 GShTh Ao, Pt, Pv, Am
42 4 3 GThL Tf, TRp, Cb, Ms
43 4 3 GShL Php, Bp, Th, VIc
44 4 3 ShThL Bp, La, Ka, VIc
45 4 4 GShThL Bh, La, Lv, Ml
46 4 4 GShThL Ao, Pl, Co, Td
47 4 4 GShThL Ao, Pv, Ka, Tp
48 4 4 GShThL Fp, Pl, Am, Ov
49 8 1 G Hl, Cc, Pt, Dg, Ao, Fr, Ap, Tf
50 8 1 Sh Bp, To, Lh, La, Gh, Vc, Pm, Pv
51 8 1 Th Ka, Ra, Dc, Lv, Co, Gm, Cb, Cj,
52 8 1 L Tp, Ov, Ms, Td, Lp, Th, Tr, Lc
53 8 2 GSh Ao, Fr, Bh, Cc, Pl, Lh, Gh, To
54 8 2 ThL Cp, Ka, Cb, Am, Lc, Td, Ml, Th
55 8 2 GTh Php, Fr, Be, Ap, Ra, Cj, Cb, Cp
56 8 2 ShL Bp, Vc, To, La, Ml, Lp, VIc, Td
57 8 3 GShTh Fp, Be, Pm, Pv, Lh, Am, Cj, TRp
58 8 3 GThL Ao, Pt, Be, Co, Lv, Ov, Th, Lc
59 8 3 GShL Cc, Php, Tf, Gh, Vc, Pm, Tr, Lc
60 8 3 ShThL Bp, Lh, Cb, Gm, Ra, Lc, Tr, Ov
61 8 4 GShThL Pt, Php, Lh, Gh, Ka, Ra, Td, Th
62 8 4 GShThL Php, Pt, To, Pm, Ra, Co, Ml, Td
63 8 4 GShThL Pt, Tf, Pl, Lh, Dc, Co, Td, Ml
64 8 4 GShThL Hl, Bh, Pl, La, Lv, Cb, Tr, Ov

transplantation of plant seedlings. The litter material geophagous earthworm species, whereas L. terrestris is
(2.53% N, C/N ratio 17.3) was collected near the site an anecic litter feeding species. Both species are among
from which the soil had been taken, dried at 608C and the dominant species at the Jena Biodiversity Experi-
cut into pieces about 3 cm in length. ment field site. Earthworms were weighed prior to
One subadult Aporrectodea caliginosa (Savigny) and placement in the microcosms (average fresh weight 863
one juvenile of Lumbricus terrestris L. were added to and 927 mg for A. caliginosa and L. terrestris, respec-
half of the microcosms. A. caliginosa is an endogeic tively). Twenty individuals of each of three Collembola

OIKOS 112:3 (2006) 515

species, Heteromurus nitidus (Leleup), Folsomia candida Soil basal respiration (ml O2 g 1 soil dry weight h1)
(Willem) and Protaphorura fimata (Gisin), were added was measured as mean of the O2 consumption rates of
to half of the microcosms creating four treatments in a unamended soil of hours 15 to 20 after start of the
two factorial design (control, with earthworms, with measurements.
Collembola, with earthworms and Collembola). The We used analysis of variance (ANOVA) as part of the
Collembola species were taken from laboratory cultures, GLM procedure in SAS 8 (SAS Inst., Cary, Florida,
where they were kept at constant temperature (178C) and USA) to test in a hierarchical order (type I sum of
fed on bakery yeast. Folsomia candida and Heteromurus squares) the effects of earthworms (E), Collembola (C),
nitidus are hemiedaphic species dwelling in the litter plant species diversity (S), plant functional group
layer and upper soil layers. H . nitidus is present at the diversity (FG) and presence/absence of legumes (L),
Jena field site. Protaphorura fimata is an euedaphic grasses (G), small herbs (Sh) and tall herbs (Th) as
species living in deeper soil layers. In total 256 micro- treatment factors. The experimental design does not
cosms were set up. allow to fully separate the effects of S and FG which are
During the experiment the microcosms were kept in a partially confounded; the F-values given in text and
temperature controlled greenhouse at a day
/night tables for the effects of S (log-linear and deviation) and
regime of 16
/8 h and 208C9/2. During the experiment FG (linear and deviation), and their interactions with
the water regime was increased from irrigating three other factors refer to those where the respective factor
times per week with 25 (week 1
/2), 40 (week 3
/5), 50 ml (and interaction) was fitted first (Neter and Wasserman
(week 5
/7) deionized water to 50 (week 8
/9) and 80 ml 1974, Schmid et al. 2002). No interaction term between S
daily (week 9
/11). and FG was calculated. The effects of presence/absence
of legumes (L), grasses (G), small herbs (Sh) and tall
herbs (Th) and there interactions with earthworms and
Collembola always were fitted after fitting S and FG. F-
Sampling and analytical procedure values of L/G interactions refer to those fitting the
After 11 weeks the earthworms were collected by hand interaction before functional groups. In analyses of
sorting, washed, dried for 1 min on filter paper and covariance (ANCOVA) plant shoot, root and total
weighed. Then, earthworms were killed by freezing, biomass were fitted as covariables to separate the effects
dried at 608C for three days and stored in a desiccator. driven by changes in plant primary production from
The anterior end of A. caliginosa without gut content diversity effects; covariables always were fitted before
was used for analysing total nitrogen concentration and fitting S and FG (and their interactions with other
15
N signatures which were determined by a coupled factors). Microbial biomass and respiration were also
system consisting of an elemental analyzer (NA 1500, analysed by ANCOVA using the soil water content as
Carlo Erba, Milan) and a gas isotope mass spectrometer covariable to control for differences caused by soil
(MAT 251, Finnegan; Reineking et al. 1993). For moisture. Interactions between factors that were not
15 significant were excluded from the model. Prior to
N atmospheric N2 served as primary standard and
acetanilide (C8H9NO; Merk, Darmstadt) as internal ANOVA data were inspected for homogeneity of var-
calibration. iance and log-transformed if required.
Collembola were sampled taking a soil core of a
diameter of 5 cm from each of the microcosms to a depth
of 5 cm. Collembola were extracted by heat (Macfadyen
1961), separated into species and counted.
Microbial biomass was measured using the substrate-
Results
induced respiration (SIR) method (Anderson and Earthworms
Domsch 1978). The microbial respiratory response to
addition of glucose was measured at hourly intervals in Survival and body weight
an electrolytic O2 microcompensation apparatus for 24 h In total, 92% of the 128 individuals of A. caliginosa
at 228C (Scheu 1992). Microbial biomass (Cmic; added survived until the end of the experiment. On
mg C g 1 soil) was measured after the addition of a average, the biomass of A. caliginosa increased by 17%,
sufficient amount of glucose as substrate in order to however, the increase was significantly more pronounced
saturate the catabolic activity of microorganisms (4 mg in presence (/25%) than in absence of Collembola
glucose g 1 soil dry weight). The maximum initial (/9%; Table 2). Furthermore, the body weight of A.
respiratory response (MIRR; mg O2 g 1 soil dry weight caliginosa increased with plant species and FG diversity
h1) was calculated as the average of the lowest three but only in treatments without Collembola (Fig. 1a, 1b).
readings within the first 11 h and microbial biomass was Shoot, root and total plant biomass (fitted as covari-
calculated as Cmic /38 /MIRR (mg Cmic g 1 soil dry ables) did not significantly affect the biomass of A .
weight) (Anderson and Domsch 1978, Beck et al. 1997). caliginosa (P /0.32, P/0.83 and P/0.34, respectively),

516 OIKOS 112:3 (2006)

Table 2. ANOVA table of F-values on the effect of Collembola (C), number of plant species (S), number of plant functional groups
(FG) and presence of legumes (L), grasses (G), small herbs (Sh) and tall herbs (Th) on changes in body weight, tissue nitrogen
concentrations and 15N atom% in Aporrectodea caliginosa.
15
Variables analysed Changes in body weight Tissue N (%) N atom%
Treatment factors

C F1/97 /15.75 P /0.0001 F1/82 /0.39 P /0.5361 F1/82 /4.54 P/0.0361

FG F3/97 /1.39 P /0.2499 F3/82 /2.21 P /0.0937 F3/82 /3.61 P/0.0167
FG linear F1/124 /2.63 P /0.1075 F1/109 /0.01 P /0.9334 F1/109 /3.34 P /0.0704
FG deviation F2/124 /0.12 P /0.8883 F2/109 /3.00 P /0.0541 F2/109 /3.00 P /0.0540
S F3/97 /5.78 P /0.0011 F3/82 /0.81 P /0.4915 F3/82 /2.62 P /0.0561
S log-linear F1/124 /8.25 P /0.0048 F1/109 /0.21 P /0.6493 F1/109 /3.64 P /0.0590
S deviation F2/124 /2.30 P /0.1048 F2/109 /0.99 P /0.3749 F2/109 /1.49 P /0.2292
L F1/97 /0.56 P /0.4543 F1/82 /3.65 P /0.0597 F1/82 /5.33 P/0.0235
G F1/97 /0.12 P /0.7249 F1/82 /0.31 P /0.5767 F1/82 /1.59 P /0.2105
Sh F1/97 /0.16 P /0.6879 F1/82 /1.29 P /0.2586 F1/82 /0.04 P /0.8370
Th F1/97 /0.49 P /0.4847 F1/82 /0.06 P /0.8049 F1/82 /1.87 P /0.1757
C/FG F3/97 /4.31 P /0.0068 F3/82 /3.09 P /0.0315 F1/82 /0.74 P /0.5287
C/S F3/97 /8.24 P B/0.0001 F3/82 /1.04 P /0.3804 F1/82 /1.00 P /0.3990
C/L F3/97 /0.78 P /0.3779 F1/82 /7.03 P /0.0096 F3/82 /8.44 P/0.0047
C/G F3/97 /0.14 P /0.3779 F3/82 /3.12 P /0.0812 F3/82 /3.28 P /0. 0738
C/Sh F3/97 /1.43 P /0.2345 F3/82 /0.18 P /0.6739 F3/82 /2.74 P /0.1017
C/Th F3/97 /0.46 P /0.4979 F3/82 /2.10 P /0,1510 F3/82 /0.25 P /0.6188
S/L F3/97 /2.93 P /0.0372 F3/82 /0.64 P /0.5905 F3/82 /2.65 P /0.0541
S/G F3/97 /3.17 P /0.0277 F3/82 /1.40 P /0.2497 F3/82 /1.13 P /0.3407
S/Sh F3/97 /0. 64 P /0.5910 F3/82 /0.61 P /0.6127 F3/82 /1.10 P /0.3534
S/Th F2/97 /2.90 P /0.0391 F2/82 /1.72 P /0.1695 F2/82 /0.65 P /0.5864

suggesting that the plant species and functional group Collembola and plant functional group diversity, with
effects were not due to increased plant biomass. legumes contributing most to this effect (Table 2). In
The percentage of L. terrestris individuals collected at presence of legumes and without Collembola earthworm
the end of the experiment was only around 60%; despite tissue 15N atom% slightly increased; in contrast, in
the 10 cm transparent fences used, some individuals presence of Collembola it decreased (Fig. 2b). Again,
managed to escape form the pots in the last weeks of the this suggests that presence of legumes provided addi-
experiment when the plants were used to evade. On tional nitrogen that diminished the competition for
average, the biomass of the surviving individuals had nitrogen between A. caliginosa and Collembola that
increased by 34%. In contrast to A. caliginosa the occurred in the absence of legumes. As a result the total
presence of Collembola did not affect the body weight earthworm N tissue content did not decrease but the 15N
of L. terrestris, but it decreased with plant species atom% declined, presumably in part through assimila-
diversity in treatments with legumes, whereas in treat- tion of nitrogen with low 15N signature typical for
ments without legumes it was at a maximum at the legume fixed nitrogen.
maximum plant species diversity (S /L interaction
F3,42 /4.06, P/0.0128; Fig. 1c).

Tissue nitrogen Collembola

Tissue nitrogen concentration was only analysed for A. Collembola densities increased during the experiment
caliginosa . It was affected by plant functional group reaching the upper range occurring in temperate grass-
diversity but only in the treatment with Collembola lands (average of 220.000 ind. m 2). Total number of
being at a minimum at the three functional group Collembola was reduced by earthworms ( /20%) and in
diversity level (significant C /FG interaction; Table 2). the presence of legumes (/23%), but was increased in
The effect of plant functional group diversity likely was the presence of grasses (/66%). Collembola species
caused by legumes (significant C/L interaction; Table responded differently to plant species diversity, func-
2); without legumes Collembola decreased the concen- tional group diversity, identity of functional groups and
tration of nitrogen in earthworm tissue from 13.1% to the presence of earthworms. Numbers of P. fimata
12.8% suggesting that Collembola and earthworms increased with plant species and functional group
competed for nitrogen resources but only if there were diversity, while that of F. candida was at a minimum in
no legumes (Fig. 2a). the two species mixtures (Table 3). Including plant root
biomass as covariable the effect of plant diversity on the
15
N incorporation density of F. candida declined (F1,94 /2.41, P/0.0720)
Incorporation of 15N from the litter was only analysed whereas in P. fimata it increased (F1,94 /8.00, P/
for A. caliginosa . Similar to tissue nitrogen concentra- 0.0057) suggesting that the plant diversity effect in part
tion the 15N atom% in A. caliginosa depended on was due to differences in root biomass in F. candida but

OIKOS 112:3 (2006) 517

(a) 0.6 (a) 14.0
0.5 13.8
Changes in body weight [g]

0.4
13.6

A.caliginosa N %
0.3
13.4
0.2
13.2
0.1
13.0
0.0
-0.1 12.8

-0.2 12.6

-0.3
ew 12.4 ew
ew + coll ew + coll
-0.4 12.2
1 2 4 8 Without With
Plant species diversity Legume presence

(b) 0.6 (b) 0.158

A. caliginosa log15 N atom %

Changes in body weight [g]

0.5 0.156
0.154
0.4
0.152
0.3
0.150
0.2 0.148

0.1 0.146
0.144
0.0
0.142
-0.1 ew ew
0.140
ew + coll ew + coll
-0.2 0.138
1 2 3 4 Without With
Functional group diversity Legume presence

(c) 1.0 Fig. 2. (a) Tissue nitrogen concentration and (b) 15N atom% of
Aporrectodea caliginosa as affected by Collembola and presence
0.9
of legumes. Error bars represent9/SE.
Changes in body weight [g]

0.8
0.7
0.6
Presence of legumes reduced the density of F. candida
0.5
( /23%) and H. nitidus (/49%), whereas grasses
0.4
increased the density of these Collembola species (/
0.3
0.2
146 and /90% for P. fimata and H. nitidus, respec-
0.1
tively). However, for H. nitidus the effect depended on
0.0
the presence of earthworms. In the presence of earth-
- leg worms grasses lead to a more than four fold higher
-0.1
+ leg
-0.2 density of H. nitidus (significant Ew /G interaction,
1 2 4 8
Table 3, Fig. 3a). Also, legumes affected the density of H.
Plant species diversity nitidus but again, the effect depended on the presence of
Fig. 1. (a) Body weight of Aporrectodea caliginosa as affected earthworms. In the presence of earthworms legumes
by plant species diversity and Collembola and (b) plant reduced the density of H. nitidus by 70% (significant
functional group diversity and Collembola, and (c) body weight
of Lumbricus terrestris as affected by plant species diversity and Ew /L interaction, Table 3, Fig. 3b).
presence of legumes. Error bars represent9/SE. Of the grass species, mixtures containing T. flavescens,
F. rubra and F. pratensis strongly increased the density
not in P. fimata . Using shoot biomass, total plant of P. fimata, suggesting that certain combinations of
biomass or the biomass ratio between different plant plant species affected the reproduction and survival of
fuctional groups per pot as covariables did not affect the Collembola. The significant interaction between legumes
plant diversity effect on P. fimata suggesting that neither and grasses reflects that the increase in Collembola
of these factors contributed to the observed effect of density in presence of grasses was less pronounced if
plant species diversity on the numbers of P. fimata. legumes were also present. Tall herbs also affected the

518 OIKOS 112:3 (2006)

Table 3. ANOVA table of F-values on the effect of earthworms (E), number of plant species (S), number of plant functional groups
(FG) and presence of legumes (L), grasses (G), small herbs (Sh) and tall herbs (Th) on the density of the Collembola species studied
(Folsomia candida , Protaphorura fimata and Heteromurus nitidus ).

Collembola F. candida P. fimata H. nitidus All three species

Treatment factors

E F1/94 /3.30 P /0.0725 F1/94 /2.55 P /0.1138 F1/94 /0.10 P /0.7535 F1/94 /6.04 P/0.0158
FG F3/94 /0.53 P /0.6634 F3/94 /3.41 P /0.0208 F3/94 /0.93 P /0.4301 F3/94 /0.87 P/0.4587
FG log linear F3/94 /3.11 P /0.0805 F1/122 /5.66 P /0.0189 F1/122 /0.01 P /0.9163 F1/122 /1.25 P/0.2655
FG deviation F3/94 /2.08 P /0.1293 F1/122 /0.84 P /0.4335 F1/122 /1.12 P /0.3309 F1/122 /0.37 P/0.6904
S F3/94 /3.18 P /0.0274 F3/94 /4.57 P /0.0050 F3/94 /0.20 P /0.8932 F3/94 /2.69 P/0.0506
S log linear F1/122 /3.17 P /0.0775 F1/122 /5.63 P /0.0192 F1/122 /0.28 P /0.5967 F1/122 /2.57 P/0.1113
S deviation F2/122 /2.38 P /0.0967 F1/122 /2.22 P /0.1128 F1/122 /0.10 P /0.9028 F1/122 /1.65 P/0.2017
L F1/94 /5.24 P /0.0243 F1/94 /1.92 P /0.1688 F1/94 /9.19 P/0.0031 F1/94 /6.44 P/0.0128
G F1/94 /0.82 P /0.3678 F1/94 /39.35 P B/0.0001 F1/94 /23.17 PB/0.0001 F1/94 /21.02 PB/0.0001
Sh F1/94 /2.87 P /0.0934 F1/94 /3.46 P /0.0662 F1/94 /0.06 P /0.8123 F1/94 /0.36 P/0.5488
Th F1/94 /2.24 P /0.1375 F1/94 /9.16 P /0.0032 F1/94 /2.38 P /0.1260 F1/94 /2.08 P/0.1522
L/G F3/94 /4.80 P /0.0037 F3/94 /16.28 P B/0.0001 F3/94 /7.92 PB/0.0001 F3/94 /7.07 P/0.0002
E /FG F3/94 /0.04 P /0.9889 F3/94 /0.46 P /0.7089 F1/94 /1.46 P /0.2304 F1/94 /0.47 P/0.7042
E /S F3/94 /2.62 P /0.0554 F3/94 /2.21 P /0.0923 F1/94 /2.15 P /0.0987 F1/94 /1.92 P/0.1319
E/L F3/94 /2.45 P /0.1209 F1/94 /0.10 P /0.7528 F3/94 /6.52 P/0.0123 F1/94 /1.11 P/0.2948
E/G F3/94 /1.08 P /0.3005 F3/94 /0.03 P /0.8715 F3/94 /6.63 P/0.0116 F3/94 /0.76 P/0.3861
E/Sh F3/94 /2.27 P /0.1350 F3/94 /0.00 P /0.9587 F3/94 /0.51 P /0.4778 F3/94 /1.22 P/0.2728
E/Th F3/97 /1.21 P /0.2747 F3/94 /0.18 P /0.6710 F3/94 /0.48 P /0.4908 F3/94 /0.67 P/0.4136
S/L F3/94 /1.32 P /0.2718 F3/94 /0.85 P /0.4722 F3/94 /1.95 P /0.1264 F3/94 /1.84 P/0.1541
S/G F3/94 /0.14 P /0.9363 F3/94 /0.79 P /0.5013 F3/94 /0.16 P /0.9210 F3/94 /0.63 P/0.6001
S/Sh F3/94 /1.28 P /0.2872 F3/94 /0.54 P /0.6555 F3/94 /1.01 P /0.3936 F3/94 /0.60 P/0.6134
S/Th F3/94 /4.56 P /0.0050 F2/94 /2.07 P /0.1089 F2/94 /0.96 P /0.4138 F3/94 /4.38 P/0.0062

density of P. fimata ; in presence of tall herbs the density Microbial biomass was only affected by earthworms;
was reduced by 25%. in the presence of earthworms it decreased on average by
Presence of earthworms generally tended to affect approximatively 4%. Including root biomass, total plant
each of the Collembola species but their effect varied biomass and the biomass ratio between plant functional
with plant species diversity (P B/0.1) for each of the groups per pot as covariables suggest that root biomass
three species (E /S interactions; Table 3). On average, contributed to the plant diversity effect on basal
the presence of earthworms reduced the density of respiration (drop of P-values to 0.0644), but these
F. candida ( /47%; Table 3) which was most pronounced parameters did not contribute to the reduction in
in the two plant species treatment ( /59%) and least microbial biomass in the presence of earthworms nor
pronounced in the one plant species treatment ( /28%), to the effect of tall herbs on soil respiration.
however, the effects were only marginally significant Data on the response of plants to decomposer
(E /S interaction, Table 3). In contrast to F. candida , P. manipulation is subject to another paper (S. Partsch,
fimata was less sensitive to the presence of earthworms. A. Milcu and S. Scheu, unpubl.). We did not find
unnaturally high root biomass in the microcosms as
compared with the field conditions.

Microorganisms
Microbial basal respiration but not microbial biomass Discussion
was significantly affected by soil water content as
indicated by ANCOVA (Table 4). The presence of Earthworms
earthworms reduced microbial basal respiration by Earthworms are considered to be strongly influenced by
17%, whereas Collembola did not affect microbial the amount of plant residues entering the soil (Edwards
respiration (Fig. 4a). Microbial basal respiration but and Bohlen 1996). Since most of the biomass produced
not microbial biomass was significantly affected by plant by plants ultimately enters the detrital system earth-
species and functional group diversity, decreasing log- worms should benefit from increased primary produc-
linearly and linearly, respectively, with the increase in tion. Since primary production increases with plant
species and functional group diversity (Fig. 4b, 4c). species richness in grassland communities (Hector
Basal respiration was at a maximum in the two species et al. 1999, Tilman et al. 2001) plant species diversity
treatment and at a minimum in the eight species likely also impacts earthworms and other decomposers.
treatment with the one and four species treatment being In fact, in field experiments Zaller and Arnone (1999)
intermediate. In the presence of tall herbs basal respira- and Spehn et al. (2000) found the biomass of earth-
tion was increased by ca 5%. worms to increase with increasing plant species richness.

OIKOS 112:3 (2006) 519

(a) 80
is difficult to differentiate between effects caused by litter
materials from above the ground from those caused by
70
root derived resources. Results of the present study
H. nitidus Ind./100 cm3

60 suggest that the increase in earthworm biomass with

50
increasing plant species diversity is largely caused by
root derived resources since the same aboveground litter
40
resources were added to each of the treatments. How-
30 ever, results of ANCOVAs suggest that the increase in
20
body weight of A. caliginosa with increase in plant
species richness was not related to root or total plant
10
- ew biomass. Presumably, the increase in earthworm body
0 + ew weight with increasing plant diversity was caused by
Without With changes in the quality rather than the quantity of
Grass presence rhizodeposits. Possibly, rhizodeposits are more diverse
in more diverse plant communities. In contrast to the
(b) study of Spehn et al. (2000), the increase in body weight
70
of A. caliginosa was not related to the presence of
H. nitidus Ind./100 cm3

60 legumes which provide shoot and root litter resources

rich in nitrogen. This supports the conclusion of Tiunov
50
and Scheu (2004) that endogeic earthworms are primar-
40 ily limited by carbon rather than nitrogen. Interestingly,
the increase in biomass of A. caliginosa in more diverse
30
plant communities was associated with an increase in the
20 exploitation of the 15N labelled litter material added to
the microcosms. This indicates that earthworms in the
10
- ew more diverse plant communities were more active and
0 + ew therefore more efficiently exploited organic resources in
Without With soil.
Legume presence A striking result of the present study was that at low
plant diversity the increase in body weight of A.
Fig. 3. Densities of Heteromurus nitidus as affected by (a) caliginosa was more pronounced in presence of Collem-
earthworms and presence of grasses and (b) earthworms and
presence of legumes. Error bars represent9/SE. bola. This suggests that Collembola facilitated the
resource acquisition by earthworms. However, as indi-
cated by tissue 15N concentrations this was not the case
In both studies this was explained by increased input of for the litter resources added to the microcosms. Also,
resources but also by changes in resource quality. In field reduced tissue nitrogen concentration of A. caliginosa in
experiments it is difficult to disentangle effects of presence of Collembola (treatments without legumes)
resource quality from those of resource quantity (Scheu suggests that Collembola and earthworms competed for
and Schaefer 1998, Maraun et al. 2001). Furthermore, it nitrogen resources which is consistent with earlier studies

Table 4. ANCOVA table of F-values on the effect of Earthworms (E), Collembola (C), number of plant species (S), number of plant
functional groups (FG) and presence of legumes (L), grasses (G), small herbs (Sh) and tall herbs (Th) on microbial basal respiration
and microbial biomass; soil water content was used as covariable.

Variables analysed Basal respiration Microbial biomass

Treatment factors

Water F1/237 /52.32 P B/0.0001 F1/237 /0.28 P /0.5947

E F1/237 /43.44 P B/0.0001 F1/237 /7.15 P/0.0080
C F1/237 /0.01 P /0.9218 F1/237 /0.87 P /0.3520
E/C F1/237 /1.76 P /0.1858 F1/237 /0.25 P /0.6173
FG F3/237 /1.34 P /0.2606 F3/237 /1.29 P /0.2771
FG linear F1/247 /9.51 P /0.0023 F1/247 /1.79 P /0.1827
FG deviation F1/247 /0.68 P /0.5078 F1/247 /1.03 P /0.3587
S F3/237 /3.13 P /0.0263 F3/237 /1.03 P /0.3787
S log linear F1/247 /5.85 P /0.0163 F1/247 /0.71 P /0.4017
S deviation F1/247 /2.47 P /0.0870 F1/247 /1.15 P /0.3169
G F1/237 /2,05 P /0.1539 F1/237 /1.53 P /0.2176
Sh F1/237 /0.52 P /0.4733 F1/237 /3.41 P /0.0662
Th F1/237 /6.95 P /0.0090 F1/237 /0.03 P /0.8733
L F1/237 /0.81 P /0.3698 F1/237 /1.70 P /0.1929

520 OIKOS 112:3 (2006)

(a) 2.4 Compared to the endogeic species A. caliginosa which
2.3 predominantly feeds on organic resources in the soil, the
2.2 anecic species L. terresris was less responsive to the
µl O2 h-1 g soil dw-1

experimental treatments. Anecic species strongly rely on

2.1
litter input form above the ground (Edwards and Bohlen
2.0
1996). Since each of the treatments was set up with the
1.9 same litter material, the lower responsiveness of L.
1.8 terrestris was expected. However, changes in body
1.7 weight of L. terrestris were also affected by plant species
1.6
diversity, but this varied significantly with the presence
of legumes. Without legumes earthworm body weight
1.5
only increased in the highest plant diversity treatment
1.4
ctr ew coll ew+coll whereas in presence of legumes it was at a maximum in
Treatment the two species treatment and then declined at higher
plant species diversity. The increase in biomass of L.
(b) 2.4 terrestris suggests that anecic earthworm species also
2.3 rely at least in part on belowground resources. The
increase in biomass at high plant species diversity (in
2.2
µl O2 h-1 g soil dw-1

absence of legumes) supports our conclusion that earth-

2.1
worms may benefit from more diverse rhizodeposits.
2.0

1.9

1.8

1.7 Collembola
1.6 In contrast to our expectation the density of Collembola
1.5 did not consistently increase with plant species diversity
1.4
nor with legume presence. Rather, the Collembola
1 2 4 8 species used differentially responded to the experimental
Plant species diversity treatments suggesting that functional groups of Collem-
bola differentially respond to plant community compo-
(c) 2.2 sition. The only species which significantly increased in
2.1 density with plant species diversity was P. fimata .
Consistently, species of the genus Protaphorura have
µl O2 h-1 g soil dw-1

2.0
been reported previously to benefit from an increase in
1.9 species diversity in a field experiment (Salamon et al.
1.8 2004). High densities of Protaphorura species in the
1.7
latter study were associated with high fine root biomass,
high microbial biomass and high soil water content. As
1.6 indicated by ANCOVAs using root biomass, microbial
1.5 biomass and soil water content as covariables these
1.4
factors were not responsible for the increased density of
P. fimata in our experiment. Rather, high density of P.
1.3
1 2 3 4 fimata (and also of H. nitidus ) was associated with the
Plant functional group diversity presence of grasses (but not grass biomass as indicated
by ANCOVA), in particular that of Trisetum flavescens,
Fig. 4. Microbial basal respiration as affected by (a) decom- Festuca rubra and Festuca pratensis. This indicates that
posers, (b) plant species diversity and (c) plant functional group
diversity. Adjusted means and standard deviation calculated the identity of functional groups (grasses) and within
using water as covariable (average water content 30.8%). Error functional groups the identity of plant species is more
bars represent9/SE. important for Collembolan performance then the diver-
sity of plant species and functional group per se.
(Scheu et al. 1999). Overall, the results indicate that the Total density of Collembola was reduced in the
relationship between earthworms and Collembola is presence of earthworms (/20%), in particular that of
complex; depending on the diversity of the plant F. candida (/46%),. As hemiedaphic species F. candida
community and the element considered (C or N). predominantly colonizes the litter layer; the reduced
Collembola may facilitate or inhibit earthworm resource density in the presence of earthworms therefore likely
acquisition. was caused by removal of litter by earthworms, in

OIKOS 112:3 (2006) 521

particular by L. terrestris. In the field, however, F. biomass. The low responsiveness of microbial biomass
candida and other hemiedaphic Collembola species have suggests that microorganisms in the soil are rather
been documented to reach high density in middens and resistant to changes in belowground resource supply.
burrows of L. terrestris (Wickenbrock and Heisler 1997, In comparison to microbial biomass, the respiratory
Maraun et al. 1999) and this was explained by enhanced activity of microorganisms responded more sensitively to
food supply and increased soil pore space. Since anecic the experimental manipulations. Similar to microbial
earthworms, such as L. terrestris, concentrate litter biomass microbial respiration was also reduced by
resources in middens but deplete it in between middens, earthworms supporting our conclusion that earthworms
increased densities of Collembola in middens presum- effectively competed with microorganisms for resources
ably occurs at the expense of the region in between in the soil. Furthermore, microbial respiration varied
middens. Since in the present experiment L. terrestris with plant species diversity and this likely was in part
consumed the litter material quickly rather than con- due to differences in root biomass. However, the
centrating it in middens, hemiedaphic Collembola were significant effect of tall herbs on microbial respiration
detrimentally affected. In contrast to F. candida , H. and the lack of correlation with root biomass suggest
nitidus benefited from the presence of earthworms when that not only belowground productivity but also the
grasses were present. In part this might have been due to quality of rhizodeposits affects microbial activity in the
competitive release caused by the reduced density of F. rhizosphere.
candida . However, since H. nitidus has been shown to
selectively colonize earthworms casts (Salmon and
Ponge 1999, Salmon 2004), more likely H. nitidus Conclusion
benefited from resources in earthworm casts deposited
The hypothesis that decomposers are beneficially
on the soil surface and in upper soil layers.
affected by an increase in plant species and functional
group diversity appears to be oversimplistic. Rather,
the response of decomposers to variations in plant
Microorganisms diversity varies with decomposer species with endogeic
Microorganisms in soil are primarily limited by the and euedaphic species, such as A. caliginosa and P.
amount of carbon entering the detrital system and fimata being more sensitive than anecic (L. terrestris )
hence by plant biomass production (Zak et al. 1994, or hemiedaphic species (F. candida and H. nitidus ).
Spehn et al. 2000). However, in our experiment Consistent with our expectations, the identity of the
microbial biomass was not related to total plant plant functional groups strongly affected growth and
biomass production but correlated weakly with root reproduction of decomposers. Grasses beneficially
biomass. This suggests that microbial biomass in soil affected Collembola densities whereas legumes detri-
(as measured by substrate-induced respiration) is resis- mentally affected Collembola densities but beneficially
tant to plant species composition (and associated affected total N concentration in A. caliginosa tissue.
belowground resource input) and to the feeding activity Also consistent with our expectations, soil macrofauna
of Collembola. In agreement with these findings it has and mesofauna species affected each other and these
been documented that even massive changes in liquid interactions were modified by plant species diversity,
carbon input (glucose) hardly affect microbial biomass plant functional group diversity and presence of
in soil (Joergensen and Scheu 1999, Maraun et al. legumes. Both changes in the amount and quality of
2001). The failure of Collembola to control the biomass belowground resources presumably were responsible for
of microorganisms in soil suggests that most of the these modifications. Future experiments need to further
microorganisms are inaccessible to microarthropod incorporate variations in the input of aboveground
grazers (Kandeler et al. 1998, Schlatte et al. 1998). In litter resources with plant species and functional group
contrast to Collembola, microbial biomass was reduced diversity to fully capture the complexity of the
in presence of earthworms suggesting that either earth- dependency of decomposers on plant community
worms digested microorganisms or effectively competed composition.
with microorganisms for resources. There is increasing Acknowledgements
/ Financial support by the German Science
evidence that the latter but not the former is in fact the Foundation is gratefully acknowledged (FOR 456; The Jena
Experiment). We also thank to Nico Eisenhauer and Diana
case (Scheu and Schaefer 1998, Schönholzer et al. 1999, Capota for help with the biomass harvest and sample analyses.
Wolter and Scheu 1999, Tiunov and Scheu 2004).
Overall, the low responsiveness of microbial biomass
to the experimental treatments suggests that the effects
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