ARTICLE IN PRESS

Basic and Applied Ecology 9 (2008) 182–188 www.elsevier.de/baae

Effects of Collembola and fertilizers on plant performance

(Triticum aestivum) and aphid reproduction (Rhopalosiphum padi)
Kirsten Schütza,, Michael Bonkowskib, Stefan Scheub
a
Departement of Environmental Sciences, Biogeography and Applied Ecology, University of Basel,
St Johanns Vorstadt 10, 4056 Basel, Switzerland
b
Institute of Zoology, Technical University of Darmstadt, Schnittspahnstr. 3, 64287 Darmstadt, Germany

Received 14 September 2005; accepted 25 July 2006

Abstract
Effects of Collembola (Protaphorura fimata) on the development of wheat (Triticum aestivum) and the reproduction
of aphids (Rhopalosiphum padi) were investigated at different soil nutrient concentrations in a laboratory experiment.
Fertilization with N and NPK increased biomass and nitrogen content of wheat, aphid reproduction and abundance of
Collembola. Presence of Collembola tended to decrease biomass of leaves and ears, and caused a delayed ear
production of the plants. Aphid reproduction was significantly reduced in the presence of Collembola (14%) and
most pronounced in fertilizer treatments. We suggest that the reduction of aphid reproduction is caused by
Collembola-mediated changes in resource allocation and growth of wheat.
r 2007 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

Zusammenfassung
In einem Laborexperiment wurde der Einfluss von Collembolen (Protaphorura fimata) auf die Entwicklung von
Weizen (Triticum aestivum) und die Reproduktion von Aphiden (Rhopalosiphum padi) in Böden mit verschiedenen
Nährstoffgehalten untersucht. Durch Düngung mit N und NPK wurden Biomasse und Stickstoffgehalt von Weizen,
die Reproduktion von Aphiden und die Abundanz von Collembolen erhöht. Collembolen verringerten tendenziell die
Biomasse von Blättern und Ähren und verzögerten die Ährenbildung. In Anwesenheit von Collembolen war die
Reproduktion von Aphiden signifikant reduziert (14%); dies war in den gedüngten Behandlungen am deutlichsten.
Die Ergebnisse deuten daraufhin, dass Collembolen durch Beeinflussung des Wachstums von Weizen die
Reproduktion von Aphiden verringern können.
r 2007 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

Keywords: Soil organisms; Soil nutrients; Herbivory; Belowground–aboveground interactions; Microcosm; Fecundity

Corresponding author. Tel.: +41 612670803; fax: +41 612670801.

E-mail address: kirsten.schuetz@unibas.ch (K. Schütz).

1439-1791/$ - see front matter r 2007 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.baae.2006.07.003
 ARTICLE IN PRESS
K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188
Introduction
Below- and aboveground processes in terrestrial
communities have usually been investigated separately
from each other but the awareness of the interrelation-
ships between below- and aboveground systems is
increasing (Wardle et al., 2004). Studies investigating
the effects of soil organisms on plants and the above-
ground system have focussed on beneficial effects caused
by mycorrhiza or detrimental effects caused by root
herbivores (Bardgett & Chan, 1999; Bezemer et al.,
2005; Harris & Boerner, 1990). However, the majority of
soil organisms derive their energy from decomposition
of soil organic matter. Since decomposers are respon-
sible for nutrient recycling, the aboveground foodweb
strongly depends on the activity of the belowground
community.
Recent studies have shown that decomposers affect
the development and reproduction of aphids (Bonkows-
ki, Geoghegan, Birch, & Griffiths, 2001; Scheu, Theen-
haus & Jones, 1999; Wurst & Jones, 2003). Aphids are
good indicators of plant quality since they are sensitive
to changes in nutrient supply within their host plants
(Dixon, 1985). Aphid development and reproduction is
known to be limited by nitrogen (Mattson, 1980;
McNeill & Southwood, 1978; VanEmden, 1966;
VanEmden & Bashford, 1969).
Collembola are the most important grazers of fungal
mycelia in soil (Lussenhop, 1992; Shaw, 1992). Collem-
bola grazing releases nutrients locked in fungal biomass
(Filser, 2002; McGonigle, 1995). In addition, moderate
grazing may keep fungi and particularly mycorrhiza in
an active state, thus further promoting plant growth
(Ek, Sjögren, Arnebrant, & Söderström, 1994; Gange,
2000). However, high grazing leads to decreasing
mycorrhizal infection and, consequently, to negative
effects on plant growth (Harris & Boerner, 1990;
Lussenhop, 1996).
Scheu et al. (1999) were the first to investigate the
effects of Collembola on the performance of aphid
herbivores. They documented that Collembola increased
aphid reproduction on the grass Poa annua by a factor
of 3, whereas aphid reproduction on the legume
Trifolium repens was reduced by about 45%. The
authors suggested that Collembola decrease aphid
reproduction on more palatable hosts with high tissue
nitrogen concentrations but increase aphid reproduction
on hosts of low food quality and low tissue nitrogen
concentrations. Presumably, Collembola increased nu-
trient availability in soil thereby facilitating the growth
of P. annua and accordingly that of aphids. By fixing
atmospheric nitrogen legumes are less dependent on soil
nutrient availability. Therefore, by mobilizing nutrients
Collembola may little affect the growth of legumes and
also that of plant sucking aphids. However, to prove
whether Collembola affect aphid reproduction via
183
increasing plant nutrient supply, studies investigating a
single plant species growing at different soil nutrient
concentrations are necessary.
To test whether the effect of Collembola on aphid
reproduction indeed varies with host nutrient status, we
investigated the effects of Collembola (Protaphorura
fimata) on aphid (Rhopalosiphum padi) reproduction
feeding on a single host species (wheat; Triticum
aestivum) grown at different nutrient regimes. Wheat
as model plant was chosen since grasses (Poaceae)
vigorously respond to soil nutrient availability. We
hypothesized that the presence of Collembola increases
aphid reproduction by enhancing nutrient availability to
unfertilized plants and that these effects resemble those
of fertilizers.
Materials and methods
Experimental set-up
The experiment was set up in 42 experimental
chambers consisting of PVC tubes (inner diameter
9.8 cm, height 20 cm). The tubes were closed at the
bottom by lids and equipped with ceramic suction cups
for drainage of leaching water. On the top of each
chamber a wire-scaffold (height 40 cm) was installed to
support plants and to fix clip cages (height 2 cm,
diameter 4 cm) for aphids.
The chambers were filled with 960 g dry wt of a
nutrient poor loamy soil (pH 7.0, 1.58% C, C/N ratio
18.2), which had been collected at a fallow site near
Darmstadt (Roßberg, Hessen, Germany). The soil was
sieved (1 cm) and defaunated from larger soil fauna by
freezing at –22 1C for 9 days. Freezing is known to
effectively kill soil arthropods including Collembola but
to little affect soil microorganisms and soil nutrient
status (Kampichler, Bruckner, Baumgarten, Berthold, &
Zechmeister-Boltenstern, 1999; Stenberg et al., 1998). A
layer of grass litter (3.7 g dry wt) was added on the top of
each microcosm. The grass material had been collected
at the same fallow site.
Seedlings of T. aestivum L. were pregrown in a climate
chamber (1872 1C, 16 h light). After 10 days, when the
plants had reached 8–10 cm, three plants were trans-
planted into each microcosm. Two days later 20
specimens of the euedaphic springtail P. fimata were
added to half (21) of the chambers. Five days later the
fertilizer treatments were established. One-third (14) of
the microcosms received distilled H2O (control), one-
third 50 ml N fertilizer (+N) and the remaining third
50 ml NPK fertilizer (+NPK). The mass ratio of
nitrogen: phosphorus: potassium was 1:1:2.5, which is
comparable to commercial fertilizers. In both fertilizer
treatments the same amount of N was added (11.6 g
NaNO3 in 1 l H2O dest.). P and K were added as
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184 K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188
K2HPO4 (10.8 g in 1 l H2O dest.). The N supply
corresponded to fertilization with 120 kg N ha1.
Clones of R. padi, originating from a single adult
aphid were reared on wheat (16 h light, 1872 1C).
Each plant (126) was equipped with one clip-cage fixed
on a leaf into which one nymph of R. padi was placed
(week 2). When the aphids started to reproduce in
weeks 3–4 one nymph of the second generation was left
while the other juveniles and the mother aphid were
removed.
During the experiment the microcosms were kept in a
climate chamber (2071 1C, 70% humidity, 16 h light of
380 mmol m2 s1). They were arranged in seven blocks
to account for environmental variation. Blocks and the
microcosms within blocks were redistributed randomly
every week. Watering was adjusted to water uptake by
the plants to ensure similar moisture conditions in
microcosms with fast and slow growing plants;
40–60 ml d1 were added to fertilized plants and
20–30 ml d1 to control plants.
Plant, Collembola and aphid analysis
Reproduction of aphids (nymphs of the second
generation) started 6–8 days after mother aphids had
been removed. Aphids were monitored every second day
for 2 weeks by counting and removing their offspring
(8 sampling dates, weeks 7–8). During the clip caging
eight aphids died for unknown reasons and were
replaced by adult aphids (second generation) kept on
wheat in control soil parallel to the experiment. Only
offspring in clip cages with the adult aphid alive were
considered for calculating aphid reproduction.
After 3 weeks, a 2 cm tip of the basal leaf was cut and
dried (60 1C, 3 days) for measuring tissue carbon and
nitrogen concentrations. Plants were harvested after 9
weeks. Aphids were removed, plant height was measured
and plants were cut 0.5 cm above the ground. Shoots,
separated in leaves, stems and ears, were dried (60 1C,
3 days) and weighed. Soil cores (diameter 5 cm, depth
10 cm) were taken, separated in two layers (0–5
and 5–10 cm) and extracted by heat to determine the
numbers of Collembola (Kempson, Lloyd, & Ghelardi,
1963). The remaining soil and the cores used for
Collembola extraction were used for determination
of root biomass. Roots were separated from soil by
washing. Leaf (week 3 and 9) and root samples (week 9)
were analysed for carbon and nitrogen content using an
element analyser (Carlo Erba, Milan, Italy).
Statistical analysis
The experiment was set up in a two-factorial design
with three levels of fertilizers (‘‘fert’’; without, with N,
with NPK) and two levels of Collembola (‘‘coll’’; with
and without) with seven replicates each.
Data on cumulative aphid reproduction, biomass of
shoots and roots, leaf nitrogen and carbon concentra-
tion were checked for homogeneity of variances (Levene
test) and analysed without transformation by a fixed
factor two-factorial analysis of variance (ANOVA; SAS
Institute, Cary, NC). Differences between means were
inspected using Tukey’s honestly significant difference
test (HSD). To analyse changes in aphid reproduction in
time we aggregated the dataset into three reproductive
periods, early increasing (sampling dates 1–2), plateau
(sampling dates 3–6) and late decreasing (sampling dates
7–8). These data were analysed by repeated measure
ANOVA using SAS.
Results
Collembola
The density of P. fimata strongly increased during the
experiment. The density of Collembola in non-fertilized
and fertilized soil increased by a factor of 23 and 58 (933
and 2254 ind. microcosm1), respectively. Collembola
density was similar in N and NPK treatments but
density in these treatments significantly exceeded that in
non-fertilized treatments (F2,18 ¼ 13.7, Po0.001). Col-
lembola predominantly inhabited the upper 5 cm of the
mineral soil (data not shown).
Plant performance
Fertilization strongly affected plant performance with
the effects of N and NPK fertilization being similar
(Fig. 1, Table 1). Fertilized plants were larger (+45%),
produced more biomass (ears +308%, leaves +184%,
stems +262%, roots +245%) and ears appeared 2 days
earlier (after 46 vs. 48 days).
Presence of Collembola negatively affected plant
performance: leaf biomass was significantly reduced
(7%) and ears appeared on average 1 day later (46.5
vs. 47.5 days; Fig. 1, Table 1). Similar to leaf biomass,
biomass of ears tended to be reduced in the presence of
Collembola.
Nitrogen concentration of fertilized plants generally
exceeded that of non-fertilized plants; however, the
difference was more pronounced early in the experiment
(week 3: +127%) than at the end of the experiment
(week 9: +20%; Fig. 2, Table 2). Nitrogen concentra-
tion in leaves depended on the presence of Collembola
and fertilizer (significant fertilizer x Collembola interac-
tion; Table 2): Collembola reduced leaf N concentration
in N-fertilized plants by 9%, but increased leaf
N concentration in NPK-fertilized plants by 15%.
N concentrations in roots increased by 20% in fertilized
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K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188 185

52
700 b
(A) (B) b 350 (C) b b
50 600 b
a b b b 300
ab
48

leaves [mg]
500
bc
bc bc

ear [mg]
days [d]

250
46 c 400
200
300
44 150 a
200 a
42 a a 100
100
40 50
ctr N NPK ctr N NPK ctr N NPK
-C +C

Fig. 1. Effects of Collembola and fertilizer on plant growth: (A) days until ears appeared, (B) ear mass, (C) leaf mass. 71C: with/
without Collembola; N: nitrogen fertilizer; NPK: nitrogen, phosphorus and potassium fertilizer; ctr: control. Bars sharing the same
letter are not significantly different (Tukey’s honestly significant difference test, Po0.05).

Table 1. ANOVA table of F-values and degrees of freedom (df) on the effect of Collembola (Coll) and fertilizer (Fertil) on plant
growth (height, ear development), plant biomass (ear, leave, stem, root) and shoot/root ratio

df Height Ear development Ear mass Leaf mass Stem mass Root mass Shoot/root ratio

Coll 1 0.99 6.15* 3.37(*) 4.22* 0.02 1.00 1.32

Fertil 2 144.7*** 12.48*** 150.32*** 274.55*** 143.63*** 107.26*** 2.65(*)
Coll  Fertil 2 0.04 0.73 1.18 1.03 0.39 0.60 0.17

***Po0.001; *Po0.05; (*)Po0.1.

leaves (week 3) leaves (week 9) roots (week 9)

7 3.5 1.2
a a
6 b b b 3.0 c a a
b bc 1.0
abc a
N concentration [%]

5 2.5 ab a
a a 0.8
4 2.0
0.6
3 a a 1.5
0.4
2 1.0

1 0.5 0.2

0 0.0 0.0
ctr N NPK ctr N NPK ctr N NPK

-C +C

Fig. 2. Effects of Collembola and fertilizer on the concentration of nitrogen in leaves (week 3+9) and roots (week 9); for legend see
Fig. 1.

treatments, while Collembola tended to reduce root effect was alleviated. Collembola did not affect C
nitrogen concentration (10%, Fig. 2, Table 2). concentrations at any time (Table 2).
Carbon concentrations in leaves differed early in the
experiment (week 3) when fertilized plants contained on Aphids
average 43.4% and 43.8% C in N and NPK treatments,
respectively, whereas non-fertilized plants contained The number of juveniles produced increased at the
40.0% C. At the end of the experiment, however, this beginning (first 3 sampling dates), then remained almost
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186 K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188

Table 2. ANOVA table of F-values and degrees of freedom Table 3. Repeated measurements (Time) ANOVA table of F-
(df) on the effect of Collembola (Coll) and fertilizer (Fertil) on values and degrees of freedom (df) on the effect of Collembola
nitrogen concentration, carbon concentration and C/N ratio of (Coll) and fertilizer (Fertil) on aphid reproduction
leaves (week 3) and of leaves and roots (week 9)
Aphid reproduction
df Leaves Leaves Roots
(week 3) (week 9) (week 9) df Within Between
subjects subjects
N content (%) effects effects
Coll 1 0.03 0.36 2.97(*)
Fertil 2 264.22*** 13.81*** 4.20* Time 2 347.40***
Coll  Fertil 2 0.26 4.67* 0.22 Time  Coll 4 0.50 Coll 6.48*
Time  Fertil 2 18.90*** Fertil 44.26***
Time  Coll  Fertil 4 1.79 Coll  Fertil 1.40
C content (%)
Coll 1 0.01 0.53 0.27 ***Po0.001, *Po0.05.
Fertil 2 35.95*** 4.28* 1.26
Coll  Fertil 2 0.03 0.3 0.77

50 c
C/N ratio bc bc

Reproduction [ind./plant]
Coll 1 0.00 0.55 1.96 40
Fertil 2 232.96*** 13.17*** 4.49* b
Coll  Fertil 2 0.03 4.29* 0.61 30

***Po0.001; *Po0.05; (*)Po0.1. a a

20

Ctr Ctr+C N N+C NPK

10
NPK+C
9
0
8
ctr N NPK
Number of juveniles / 2 days

7 HSD
6 -C +C
5

4 Fig. 4. Effects of Collembola and fertilizer on the cumulative

3
reproduction of Rhopalosiphum padi on wheat; F1,37 ¼ 6.65,
P ¼ 0.014 for Collembola and F2,37 ¼ 68.9, Po0.001 for
2
fertilizer; for legend see Fig. 1.
1

0
09.03. 11.03. 13.03. 15.03. 17.03. 19.03. 21.03. 23.03.
sampling date

Fig. 3. Number of juveniles produced by Rhopalosiphum padi

on eight sampling dates in week 7 and 8 (interval: 2 days). C: Discussion
Collembola; N: nitrogen fertilizer; NPK: nitrogen, phosphorus
and potassium fertilizer; ctr: control; HSD, Tukey’s honestly Collembola
significant difference at Po0.05.
In terrestrial ecosystems Collembola reach densities of
constant (sampling dates 4–6) and decreased later (last 2 104–105 ind. m2 (Hopkin, 1997; Petersen & Luxton,
sampling dates) (Fig. 3, Table 3). This pattern was more 1982). Due to patchy distribution the local abundance
pronounced in fertilized treatments. Throughout the may be considerably higher (Curry, 1993). In this
experiment aphid reproduction on non-fertilized plants experiment P. fimata increased in density by a factor of
was lower than on fertilized plants. On average aphid 23 and 58 in unfertilized and fertilized treatments,
reproduction on fertilized plants was more than doubled respectively, reaching densities equivalent to 15,330 in-
compared to non-fertilized plants with 18, 39 and 46 d. m2 in the control and 37,060 ind. m2 in N and NPK
juveniles per plant in control, N and NPK treatments, treatments. These high densities may be explained by the
respectively. Overall, the presence of Collembola sig- absence of competitors, such as earthworms, and pre-
nificantly reduced cumulative reproduction of R. padi by dators, such as gamasid mites and spiders. Furthermore,
–23% and –12% in N and NPK treatments, respectively resources provided by plants, such as rhizodeposits, may
(F1,37 ¼ 6.65, P ¼ 0.014 for the effect of Collembola; have beneficially affected Collembola. Increased plant
Fig. 4). growth in fertilizer treatments presumably caused an
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K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188
increase in microbial biomass, especially fungi, a major
food resource of Collembola. Also, the regular watering
contributed to favourable environmental conditions for
Collembola.
As expected, fertilizer addition strongly increased
plant growth. From the start of the experiment fertilized
plants were higher, had more leaves and ears were
produced earlier. At the end of the experiment, plant
tissue nitrogen concentration was increased and total
biomass was more than doubled. Obviously, the plants
were limited by nitrogen and strongly benefited from N
and NPK fertilization.
Collembola also modified plant growth; they tended
to reduce plant biomass, particularly that of leaves and
caused a delay in the production of ears. Also, leaf
nitrogen concentration was affected by Collembola
(week 9), but the effect varied with fertilizer treatments.
Collembola increased shoot nitrogen concentrations in
treatments with NPK fertilization but decreased them in
treatments with N fertilization.
Detrimental effects of Collembola on plant develop-
ment have been documented previously: root biomass of
P. annua was reduced in the presence of Heteromorus
nitidus and Onychiurus scotarius (Scheu et al., 1999).
Below- and aboveground biomass of Nardus stricta
decreased in the presence of Onychiurus procampatus
(Bardgett & Chan, 1999) and high densities of Folsomia
candida caused a decrease in biomass of Geranium
robertianum (Harris & Boerner, 1990). Finlay (1985) and
Warnock, Fitter, and Usher (1982) reported that high
densities of Collembola reduced the mycorrhizal infec-
tion of plant roots, which in turn reduced plant growth
and also tended to reduce root nitrogen concentration.
However, reduced mycorrhizal infection caused by
Collembola may not uniformly result in reduced plant
growth (Kaiser & Lussenhop, 1991; Larsen & Jakobsen,
1996). Rather, mycorrhiza have been documented to
benefit from low grazing by Collembola leading to
increased plant growth (Finlay, 1985; Harris & Boerner,
1990; Warnock et al., 1982).
Aphids
Fertilization benefited plant growth and development,
and simultaneously, aphid reproduction was almost
doubled on fertilized plants throughout the experiment.
It is known that aphids benefit from increased plant
nitrogen concentration (VanEmden, 1966; VanEmden &
Bashford, 1969), but plant tissue nitrogen concentration
may not necessarily reflect nitrogen availability to
aphids. Aphids rely on nitrogen in phloem sap and the
nitrogen concentration therein may be poorly related to
that in plant tissue (Dixon, 1985). Probably, fertilization
increased both plant tissue and phloem sap nitrogen
concentrations.
187
In contrast to our expectations Collembola signifi-
cantly reduced the reproduction of R. padi, which was
most pronounced in fertilizer treatments. The Collem-
bola-mediated reduction in aphid reproduction was not
related to the nitrogen concentration in plant leaves.
Collembola reduced plant tissue nitrogen concentration
in N treatments but increased it in NPK treatments,
whereas aphid reproduction was reduced uniformly in
both treatments. Again, tissue nitrogen concentration
may not adequately reflect the nitrogen supply to
aphids, because they feed on phloem sap. Presumably,
the Collembola-mediated changes in plant performance
altered phloem chemistry and/or leaf texture leading to
reduced aphid reproduction (cf. Gange & West, 1994).
Possibly, intensive grazing of Collembola reduced
mycorrhizal infection of plant roots (Bakonyi et al.,
2002) in fertilizer treatments, thereby also changing
nutrient availability and composition for the plants and,
consequently, decreasing plant and aphid performance
(Gange, Bower & Brown, 1999; Gange & West, 1994).
However, in unfertilized treatments, grazing by Collem-
bola was low and shoot nitrogen concentration was
high, but this did not promote aphid performance.
In conclusion, addition of fertilizer increased the
biomass production of plants but simultaneously plants
became more susceptible for herbivores. Presence of
Collembola counteracted this increased susceptibility.
Future studies need to evaluate whether this counter-
action was solely caused by reduced plant performance
or an increased resistance of wheat against aphid
herbivores. There is increasing evidence that plant
resistance to aboveground herbivores is increased by
soil invertebrates including root herbivores (Bezemer &
Van Dam, 2005; van Dam et al., 2003) and also
decomposers (Wurst, Dugassa-Gobena, Langel, Bon-
kowski, & Scheu, 2004). The results contradict the
traditional view that decomposers affect plant growth
and herbivore performance only by nutrient-based
effects. Collembola most significantly affected wheat
growth and aphid reproduction in fertilizer treatments,
i.e. at high nutrient availability to plants. The results
suggest that the maintenance of a biologically active and
diverse soil fauna may significantly contribute to crop
pest control.
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