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Basic and Applied Ecology 9 (2008) 182–188

Effects of Collembola and fertilizers on plant performance

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

Received 14 September 2005; accepted 25 July 2006

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.

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: (K. Schütz).

1439-1791/$ - see front matter r 2007 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188 183

Introduction increasing plant nutrient supply, studies investigating a

single plant species growing at different soil nutrient
Below- and aboveground processes in terrestrial concentrations are necessary.
communities have usually been investigated separately To test whether the effect of Collembola on aphid
from each other but the awareness of the interrelation- reproduction indeed varies with host nutrient status, we
ships between below- and aboveground systems is investigated the effects of Collembola (Protaphorura
increasing (Wardle et al., 2004). Studies investigating fimata) on aphid (Rhopalosiphum padi) reproduction
the effects of soil organisms on plants and the above- feeding on a single host species (wheat; Triticum
ground system have focussed on beneficial effects caused aestivum) grown at different nutrient regimes. Wheat
by mycorrhiza or detrimental effects caused by root as model plant was chosen since grasses (Poaceae)
herbivores (Bardgett & Chan, 1999; Bezemer et al., vigorously respond to soil nutrient availability. We
2005; Harris & Boerner, 1990). However, the majority of hypothesized that the presence of Collembola increases
soil organisms derive their energy from decomposition aphid reproduction by enhancing nutrient availability to
of soil organic matter. Since decomposers are respon- unfertilized plants and that these effects resemble those
sible for nutrient recycling, the aboveground foodweb of fertilizers.
strongly depends on the activity of the belowground
Recent studies have shown that decomposers affect Materials and methods
the development and reproduction of aphids (Bonkows-
ki, Geoghegan, Birch, & Griffiths, 2001; Scheu, Theen- Experimental set-up
haus & Jones, 1999; Wurst & Jones, 2003). Aphids are
good indicators of plant quality since they are sensitive The experiment was set up in 42 experimental
to changes in nutrient supply within their host plants chambers consisting of PVC tubes (inner diameter
(Dixon, 1985). Aphid development and reproduction is 9.8 cm, height 20 cm). The tubes were closed at the
known to be limited by nitrogen (Mattson, 1980; bottom by lids and equipped with ceramic suction cups
McNeill & Southwood, 1978; VanEmden, 1966; for drainage of leaching water. On the top of each
VanEmden & Bashford, 1969). chamber a wire-scaffold (height 40 cm) was installed to
Collembola are the most important grazers of fungal support plants and to fix clip cages (height 2 cm,
mycelia in soil (Lussenhop, 1992; Shaw, 1992). Collem- diameter 4 cm) for aphids.
bola grazing releases nutrients locked in fungal biomass The chambers were filled with 960 g dry wt of a
(Filser, 2002; McGonigle, 1995). In addition, moderate nutrient poor loamy soil (pH 7.0, 1.58% C, C/N ratio
grazing may keep fungi and particularly mycorrhiza in 18.2), which had been collected at a fallow site near
an active state, thus further promoting plant growth Darmstadt (Roßberg, Hessen, Germany). The soil was
(Ek, Sjögren, Arnebrant, & Söderström, 1994; Gange, sieved (1 cm) and defaunated from larger soil fauna by
2000). However, high grazing leads to decreasing freezing at –22 1C for 9 days. Freezing is known to
mycorrhizal infection and, consequently, to negative effectively kill soil arthropods including Collembola but
effects on plant growth (Harris & Boerner, 1990; to little affect soil microorganisms and soil nutrient
Lussenhop, 1996). status (Kampichler, Bruckner, Baumgarten, Berthold, &
Scheu et al. (1999) were the first to investigate the Zechmeister-Boltenstern, 1999; Stenberg et al., 1998). A
effects of Collembola on the performance of aphid layer of grass litter (3.7 g dry wt) was added on the top of
herbivores. They documented that Collembola increased each microcosm. The grass material had been collected
aphid reproduction on the grass Poa annua by a factor at the same fallow site.
of 3, whereas aphid reproduction on the legume Seedlings of T. aestivum L. were pregrown in a climate
Trifolium repens was reduced by about 45%. The chamber (1872 1C, 16 h light). After 10 days, when the
authors suggested that Collembola decrease aphid plants had reached 8–10 cm, three plants were trans-
reproduction on more palatable hosts with high tissue planted into each microcosm. Two days later 20
nitrogen concentrations but increase aphid reproduction specimens of the euedaphic springtail P. fimata were
on hosts of low food quality and low tissue nitrogen added to half (21) of the chambers. Five days later the
concentrations. Presumably, Collembola increased nu- fertilizer treatments were established. One-third (14) of
trient availability in soil thereby facilitating the growth the microcosms received distilled H2O (control), one-
of P. annua and accordingly that of aphids. By fixing third 50 ml N fertilizer (+N) and the remaining third
atmospheric nitrogen legumes are less dependent on soil 50 ml NPK fertilizer (+NPK). The mass ratio of
nutrient availability. Therefore, by mobilizing nutrients nitrogen: phosphorus: potassium was 1:1:2.5, which is
Collembola may little affect the growth of legumes and comparable to commercial fertilizers. In both fertilizer
also that of plant sucking aphids. However, to prove treatments the same amount of N was added (11.6 g
whether Collembola affect aphid reproduction via NaNO3 in 1 l H2O dest.). P and K were added as
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 with NPK) and two levels of Collembola (‘‘coll’’; with
corresponded to fertilization with 120 kg N ha1. and without) with seven replicates each.
Clones of R. padi, originating from a single adult Data on cumulative aphid reproduction, biomass of
aphid were reared on wheat (16 h light, 1872 1C). shoots and roots, leaf nitrogen and carbon concentra-
Each plant (126) was equipped with one clip-cage fixed tion were checked for homogeneity of variances (Levene
on a leaf into which one nymph of R. padi was placed test) and analysed without transformation by a fixed
(week 2). When the aphids started to reproduce in factor two-factorial analysis of variance (ANOVA; SAS
weeks 3–4 one nymph of the second generation was left Institute, Cary, NC). Differences between means were
while the other juveniles and the mother aphid were inspected using Tukey’s honestly significant difference
removed. test (HSD). To analyse changes in aphid reproduction in
During the experiment the microcosms were kept in a time we aggregated the dataset into three reproductive
climate chamber (2071 1C, 70% humidity, 16 h light of periods, early increasing (sampling dates 1–2), plateau
380 mmol m2 s1). They were arranged in seven blocks (sampling dates 3–6) and late decreasing (sampling dates
to account for environmental variation. Blocks and the 7–8). These data were analysed by repeated measure
microcosms within blocks were redistributed randomly ANOVA using SAS.
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.

The density of P. fimata strongly increased during the

experiment. The density of Collembola in non-fertilized
Plant, Collembola and aphid analysis
and fertilized soil increased by a factor of 23 and 58 (933
and 2254 ind. microcosm1), respectively. Collembola
Reproduction of aphids (nymphs of the second
density was similar in N and NPK treatments but
generation) started 6–8 days after mother aphids had
density in these treatments significantly exceeded that in
been removed. Aphids were monitored every second day
non-fertilized treatments (F2,18 ¼ 13.7, Po0.001). Col-
for 2 weeks by counting and removing their offspring
(8 sampling dates, weeks 7–8). During the clip caging lembola predominantly inhabited the upper 5 cm of the
mineral soil (data not shown).
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 Plant performance
offspring in clip cages with the adult aphid alive were
considered for calculating aphid reproduction. Fertilization strongly affected plant performance with
After 3 weeks, a 2 cm tip of the basal leaf was cut and the effects of N and NPK fertilization being similar
dried (60 1C, 3 days) for measuring tissue carbon and (Fig. 1, Table 1). Fertilized plants were larger (+45%),
nitrogen concentrations. Plants were harvested after 9 produced more biomass (ears +308%, leaves +184%,
weeks. Aphids were removed, plant height was measured stems +262%, roots +245%) and ears appeared 2 days
and plants were cut 0.5 cm above the ground. Shoots, earlier (after 46 vs. 48 days).
separated in leaves, stems and ears, were dried (60 1C, Presence of Collembola negatively affected plant
3 days) and weighed. Soil cores (diameter 5 cm, depth performance: leaf biomass was significantly reduced
10 cm) were taken, separated in two layers (0–5 (7%) and ears appeared on average 1 day later (46.5
and 5–10 cm) and extracted by heat to determine the vs. 47.5 days; Fig. 1, Table 1). Similar to leaf biomass,
numbers of Collembola (Kempson, Lloyd, & Ghelardi, biomass of ears tended to be reduced in the presence of
1963). The remaining soil and the cores used for Collembola.
Collembola extraction were used for determination Nitrogen concentration of fertilized plants generally
of root biomass. Roots were separated from soil by exceeded that of non-fertilized plants; however, the
washing. Leaf (week 3 and 9) and root samples (week 9) difference was more pronounced early in the experiment
were analysed for carbon and nitrogen content using an (week 3: +127%) than at the end of the experiment
element analyser (Carlo Erba, Milan, Italy). (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-
Statistical analysis tion; Table 2): Collembola reduced leaf N concentration
in N-fertilized plants by 9%, but increased leaf
The experiment was set up in a two-factorial design N concentration in NPK-fertilized plants by 15%.
with three levels of fertilizers (‘‘fert’’; without, with N, N concentrations in roots increased by 20% in fertilized
K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188 185

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

leaves [mg]
bc bc

ear [mg]
days [d]

46 c 400
44 150 a
200 a
42 a a 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
3 a a 1.5
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
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


Ctr Ctr+C N N+C NPK

ctr N NPK
Number of juveniles / 2 days

6 -C +C

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

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
fertilizer; for legend see Fig. 1.

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
K. Schütz et al. / Basic and Applied Ecology 9 (2008) 182–188 187

increase in microbial biomass, especially fungi, a major In contrast to our expectations Collembola signifi-
food resource of Collembola. Also, the regular watering cantly reduced the reproduction of R. padi, which was
contributed to favourable environmental conditions for most pronounced in fertilizer treatments. The Collem-
Collembola. bola-mediated reduction in aphid reproduction was not
As expected, fertilizer addition strongly increased related to the nitrogen concentration in plant leaves.
plant growth. From the start of the experiment fertilized Collembola reduced plant tissue nitrogen concentration
plants were higher, had more leaves and ears were in N treatments but increased it in NPK treatments,
produced earlier. At the end of the experiment, plant whereas aphid reproduction was reduced uniformly in
tissue nitrogen concentration was increased and total both treatments. Again, tissue nitrogen concentration
biomass was more than doubled. Obviously, the plants may not adequately reflect the nitrogen supply to
were limited by nitrogen and strongly benefited from N aphids, because they feed on phloem sap. Presumably,
and NPK fertilization. the Collembola-mediated changes in plant performance
Collembola also modified plant growth; they tended altered phloem chemistry and/or leaf texture leading to
to reduce plant biomass, particularly that of leaves and reduced aphid reproduction (cf. Gange & West, 1994).
caused a delay in the production of ears. Also, leaf Possibly, intensive grazing of Collembola reduced
nitrogen concentration was affected by Collembola mycorrhizal infection of plant roots (Bakonyi et al.,
(week 9), but the effect varied with fertilizer treatments. 2002) in fertilizer treatments, thereby also changing
Collembola increased shoot nitrogen concentrations in nutrient availability and composition for the plants and,
treatments with NPK fertilization but decreased them in consequently, decreasing plant and aphid performance
treatments with N fertilization. (Gange, Bower & Brown, 1999; Gange & West, 1994).
Detrimental effects of Collembola on plant develop- However, in unfertilized treatments, grazing by Collem-
ment have been documented previously: root biomass of bola was low and shoot nitrogen concentration was
P. annua was reduced in the presence of Heteromorus high, but this did not promote aphid performance.
nitidus and Onychiurus scotarius (Scheu et al., 1999). In conclusion, addition of fertilizer increased the
Below- and aboveground biomass of Nardus stricta biomass production of plants but simultaneously plants
decreased in the presence of Onychiurus procampatus became more susceptible for herbivores. Presence of
(Bardgett & Chan, 1999) and high densities of Folsomia Collembola counteracted this increased susceptibility.
candida caused a decrease in biomass of Geranium Future studies need to evaluate whether this counter-
robertianum (Harris & Boerner, 1990). Finlay (1985) and action was solely caused by reduced plant performance
Warnock, Fitter, and Usher (1982) reported that high or an increased resistance of wheat against aphid
densities of Collembola reduced the mycorrhizal infec- herbivores. There is increasing evidence that plant
tion of plant roots, which in turn reduced plant growth resistance to aboveground herbivores is increased by
and also tended to reduce root nitrogen concentration. soil invertebrates including root herbivores (Bezemer &
However, reduced mycorrhizal infection caused by Van Dam, 2005; van Dam et al., 2003) and also
Collembola may not uniformly result in reduced plant decomposers (Wurst, Dugassa-Gobena, Langel, Bon-
growth (Kaiser & Lussenhop, 1991; Larsen & Jakobsen, kowski, & Scheu, 2004). The results contradict the
1996). Rather, mycorrhiza have been documented to traditional view that decomposers affect plant growth
benefit from low grazing by Collembola leading to and herbivore performance only by nutrient-based
increased plant growth (Finlay, 1985; Harris & Boerner, effects. Collembola most significantly affected wheat
1990; Warnock et al., 1982). 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
Aphids diverse soil fauna may significantly contribute to crop
pest control.
Fertilization benefited plant growth and development,
and simultaneously, aphid reproduction was almost
doubled on fertilized plants throughout the experiment.
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