PLANT-ANIMAL INTERACTIONS - ORIGINAL RESEARCH

Multitrophic effects of experimental changes in plant diversityon cavity-nesting bees, wasps, and their parasitoids

Anne Ebeling • Alexandra-Maria Klein •

Wolfgang W. Weisser • Teja Tscharntke

Received: 5 July 2010 / Accepted: 8 November 2011 / Published online: 26 November 2011

� Springer-Verlag 2011

Abstract Plant diversity changes can impact the abun-

dance, diversity, and functioning of species at higher tro-

phic levels. We used an experimental gradient in grassland

plant diversity ranging from 1 to 16 plant species to study

multitrophic interactions among plants, cavity-nesting bees

and wasps, and their natural enemies, and analysed brood

cell density, insect diversity (species richness), and bee and

wasp community similarity over two consecutive years.

The bee and wasp communities were more similar among

the high (16 species) diversity plots than among plots of the

lower diversity levels (up to 8 species), and a more similar

community of bees and wasps resulted in a more similar

community of their parasitoids. Plant diversity, which was

closely related to flower diversity, positively and indirectly

affected bee diversity and the diversity of their parasitoids

via increasing brood cell density of bees. Increasing plant

diversity directly led to higher wasp diversity. Parasitism

rates of bees and wasps (hosts) were not affected by plant

diversity, but increased with the diversity of their respec-

tive parasitoids. Decreases in parasitism rates of bees arose

from increasing brood cell density of bees (hosts), whereas

decreasing parasitism rates of wasps arose from increasing

wasp diversity (hosts). In conclusion, decreases in plant

diversity propagated through different trophic levels: from

plants to insect hosts to their parasitoids, decreasing density

and diversity. The positive relationship between plant

diversity and the community similarity of higher trophic

levels indicates a community-stabilising effect of high

plant diversity.

Keywords Community similarity � Hymenoptera �Jena Experiment � Structural equation model � Wild bees

Introduction

In response to recent, global declines in biodiversity (e.g.

Robinson and Sutherland 2002; Foley et al. 2005; Bies-

meijer et al. 2006), many studies have focussed on the

consequences of species loss for biotic interactions and

associated ecosystem functioning (Naeem et al. 1994;

Tilman et al. 1996; Montoya et al. 2003; Tscharntke et al.

2005; Balvanera et al. 2006; Cardinale et al. 2006; Tyli-

anakis et al. 2007). For example, starting with Mac Arthur

(1955) and Elton (1958), ecosystems stability has been

predicted to depend on diversity, and contrasting results

over the past decades have led to debate about stabilising

effects of increasing diversity (May 1972; McCann 2000).

Much of this work discussed the impact of plant species

Communicated by Roland Brandl.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s00442-011-2205-8) contains supplementarymaterial, which is available to authorized users.

A. Ebeling � A.-M. Klein � T. Tscharntke

Department of Crop Sciences,

Griesebachstr. 6, 37077 Gottingen, Germany

A. Ebeling (&) � W. W. Weisser

Institute of Ecology, University of Jena,

Dornburger Str. 159, 07743 Jena, Germany

e-mail: anne.ebeling@uni-jena.de

A.-M. Klein

Institute of Ecology, University of Luneburg,

Scharnhorststr. 1, 21335 Luneburg, Germany

Present Address:W. W. Weisser

Department of Ecology and Ecosystem Management,

Technical University of Munich,

Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany

123

Oecologia (2012) 169:453–465

DOI 10.1007/s00442-011-2205-8

loss on the stability of ecosystems (MacArthur 1955; Elton

1958; May 1972; Pimm 1991; Naem and Li 1997; Loreau

et al. 2003), and numerous studies showed that a decline in

plant species richness (hereafter, plant diversity) results in

lower ecosystem functioning and stability (e.g. Balvanera

et al. 2006; Hooper et al. 2005).

With respect to plant–insect interactions, a large number

of studies have analysed the relationship between plant

diversity and insect abundance and diversity (e.g. Siemann

1998; Haddad et al. 2001; Potts 2006; Albrecht et al. 2007;

Haddad et al. 2009; Petermann et al. 2010; Weiner et al.

2011), and two hypotheses explaining those patterns are the

resource heterogeneity hypothesis (RHH; Hutchinson

1959; Southwood et al. 1979) and the more individuals

hypothesis (MIH; Srivastava and Lawton 1998). RHH

predicts within a given area higher resource heterogeneity

with increasing diversity, leading to a greater number of

consumer species. MIH explains higher consumer abun-

dance in diverse habitats with increased food resource

availability (plant productivity, e.g. for herbivorous spe-

cies; arthropod abundance, e.g. for predators; flowers, e.g.

for bees), as has been found in previous studies (e.g. Knops

et al. 1999; Ebeling et al. 2008; Marquard et al. 2009;

Haddad et al. 2011). Increases in the consumer abundance

in turn are predicted to increase consumer diversity.

The importance of plant diversity for interactions

involving two and more trophic level is known (e.g. Albr-

echt et al. 2007; Tylianakis et al. 2007). But in the pre-

dominant part of the existing studies, mostly effects of plant

diversity on the first trophic level (herbivores) were studied

(e.g. Scherber et al. 2006) or multiple trophic levels were

mostly sampled separately without directly assessing the

interactions (Knops et al.1999; Haddad et al. 2001, 2009;

Scherber et al. 2010, but see Petermann et al. 2010).

However, the effect of plant diversity loss in a multi-trophic

context has rarely been studied (Duffy et al. 2007; Thebault

et al. 2007) and still little is known about stabilising effects

in a multitrophic level context (but see Haddad et al. 2011).

To expand this state of knowledge, we studied cavity-

nesting hymenoptera along a plant diversity gradient.

Traps for cavity-nesting hymenoptera are a suitable

system to study complex multitrophic interactions due to

their small size, high species richness, trophic complexity,

and because of their importance for ecosystem functioning

(Tscharntke et al. 1998; Klein et al. 2007; Tylianakis et al.

2007). Bees can act as pollinators for many wild and crop

plant species (Ashmann et al. 2004; Klein et al. 2007) using

flowers as their food resources. Host wasps can function as

predators, using arthropods (e.g. aphids, spiders or lepi-

doptera) as food resources. Food resources for both guilds

depend on plant diversity (Knops et al. 1999; Hegland and

Boeke 2006; Ebeling et al. 2008; Scherber et al. 2010).

Parasitoids can help to regulate insect population densities,

as their respective hosts serve as food resource. Hence, all

three functional guilds have important links to their next

trophic partner in terrestrial ecosystems (LaSalle and

Gould 1993).

We studied bees and wasps nesting in exposed reed

internodes and the interactions with their natural enemies

along a gradient in plant diversity in ‘‘The Jena Experi-

ment’’. We tested the following hypotheses:

1. Plant diversity changes affect community similarity,

diversity, and brood cell density of cavity-nesting hosts

and parasitoids. Increases in plant diversity could lead

to a broader number of niches (food resources for bees,

habitats for arthropods for wasps), increasing attrac-

tiveness for a higher number and diversity of hosts.

This may cause higher community similarity of diverse

plots. Brood cell density is a measure of consumer

abundance and thus can be used to test the more

individual hypotheses.

2. Changes in plant diversity directly affect cavity-

nesting host species (see above), as plant diversity

increases the availability of their food resources

(arthropods and flowers), with indirect effects (host-

mediated) on parasitoids and parasitism rates.

Materials and methods

Study system

Around 5% of all bees and wasps are potential cavity-

nesting species (Gathmann 1998; Veddeler et al. 2010).

Cavity-nesting bees and wasps have a solitary life-cycle

and in temperate regions mostly have one generation per

year. The most common bee species found in trap nests

across the world belong to the bee family Megachilidae

(leaf-cutting bees); the most common wasp families in trap

nests are Eumenidae (mason wasps), Sphecidae (digger

wasps), and Pompilidae (spider wasps). Larvae of leaf-

cutting bees feed on nectar, whereas larvae of mason wasps

feed mainly on caterpillars, aphids or other arthropods,

whilst larvae of digger wasps consume spiders or aphids,

and larvae of spider wasps feed on spiders (Gathmann

1998; Tscharntke et al. 1998; Tylianakis et al. 2005; Klein

et al. 2006).

Both bees and wasps (hosts) are attacked by two groups

of natural enemies: parasitoids and kleptoparasites.

Whereas parasitoids mainly consist of small wasps of the

families Braconidae, Chalcididae, Eulophidae, Ichneu-

monidae and feed on larvae, kleptoparasites do not directly

feed on bees and wasps but on their food resource, and

therefore constitute competitors of bees and wasps. Dom-

inant kleptoparasites are cuckoo wasps of the family

454 Oecologia (2012) 169:453–465

123

Chrysididae, but some species of Diptera (Bombyliidae,

Drosophilidae and Tachinidae) and Coleoptera (Dermesti-

dae, Meloidae, Mordellidae) also feed on larval food

(Veddeler et al. 2010). Even if both groups of natural

enemies have different positions in the food web, we

summarised them, as they are quite similar in their eco-

logical impact: both feeding on food resources of the host

larvae and feeding the host larvae lead to the death of a

host’s offspring. Separating both groups would lead to

lower sample sizes, making the analysis less reliable.

Henceforth, we referred to them as ‘‘parasitoids’’.

Study site

This study was carried out in ‘‘The Jena Experiment’’

(Thuringia, Germany, 50�550N, 11�350E; 130 m above sea

level). The study site was established in May 2002 and is

located in the floodplain of the river Saale. The plant

communities were sown in 78 large plots of 20 9 20 m

with a gradient of species richness (1, 2, 4, 8 and 16) per

plot (Roscher et al. 2004). The particular species mixtures

were randomly selected from a species pool of 60 common

grassland species (Roscher et al. 2004). Sown and realized

numbers of target species showed a high correlation

(Marquard et al. 2009). Hence, we used the number of

sown plant species for our analysis (henceforth, plant

diversity).

Monocultures, 2-species mixtures, 4-species mixtures,

and 8-species mixtures are represented with 16 replicates

each and 16-species mixtures with 14 replicates (total 78

plots). Replicates for each plant diversity level represent

different species compositions, by a random selection from

the species pool. An abiotic gradient in soil parameters

perpendicular to the river Saale was taken into account by

arranging plots in four blocks (Roscher et al. 2004). Dif-

ferences in the surrounding habitat of the plots were taken

into account by classifying the type of the adjacent source

habitat. Plots were either within the experimental field site

without adjacent source habitat or at the edge of the

experimental field site with adjacent source habitat or river

bank (meadow or river).

All plots are mown twice per year, a management

regime common for such meadows. We counted the

number of flowering species monthly from May to August

in both years to assess the number of plant species flow-

ering (henceforth, flower diversity) during the nest-build-

ing period and estimated the blossom cover per plot of all

flowering species. Aboveground community biomass was

harvested twice per year (during peak standing biomass in

late May and in late August) in 2005 and 2006 on all 78

large plots. This was done by clipping the vegetation at

3 cm above ground in four (only three in May 2005)

rectangles of 0.2 9 0.5 m.

In 2005 and 2006, sown species cover was visually

estimated twice a year just before biomass harvest (late May

and in late August). Single species cover data were esti-

mated using the cover classes 0: species missing; 1: B1%; 2

:1% \ x B 5%; 10: 5% \ x B 15%; 20: 15% \ x B 25%;

30: 25% \ x B 35%; 40: 35% \ x B 45%; 50: 45% \ x

B 55%; 60: 55% \ x B 65%; 70: 65% \ x B 75%; 80:

75% \ x B 85%; 90: [85%. Measurements were taken in

one 3 9 3 m area in the core area of each of the 78 large

experimental plot. For details in methods of sampling

community biomass and estimating community species

specific cover data, see Weigelt et al. (2009).

Trap nests

To study the influence of plant diversity on cavity-nesting

hymenoptera, we placed nesting traps in all 78 plots. We

made traps from a plastic tube with a diameter of 11 cm

and a length of 20 cm, filled with around 150 internodes of

the common reed Phragmites australis (Cav.) Trin. We cut

the internodes to a length of 20 cm and prepared a mix of

different diameters ranging from 2 to 10 mm (Tscharntke

et al. 1998). As protection from rain, we built wooden roofs

(50 9 50 cm) above the trap nests. In each plot, we

installed one wooden post of 1.5 m height, each with four

nesting traps. We exposed traps from the end of April to

September in 2005 and 2006, respectively. In both study

years, we sampled all nesting traps in the middle of Sep-

tember and stored them at 4�C for 12 weeks to mimic a

hibernation phase. All reed internodes with nests of bees or

wasps (identified by the species-specific nest closure at top

of the internodes) were removed. The internodes were

opened, and we made a preliminary identification of the

insect to the genus level (based on the structure of larvae or

cocoon) (Gathmann and Tscharntke 1999) and reared nests

separately in glass tubes for adults to emerge for final

identification. For each nest, we noted the number of intact

and parasitised brood cells, the number and identity of host

species, and the number and identity of parasitoid species.

Species identification

We identified Megachilidae based on Scheuchl (2006) and

Colletidae according to Amiet (1999). For identification of

eumenid and specid wasps, we used Schmid-Egger (1995)

and Dollfuss (1991). Most common parasitoid species were

identified with an unpublished identification key for trap-

nesting hymenoptera of the Agroecology Group, Gottin-

gen, Germany. The kleptoparasitic wasps of the family

Chrysididae were identified based on Kunz (1994) and

Linsenmaier (1997). Some parasitoid species (see Table 1)

could only be identified to family level, according to

Bahrmann (1995).

Oecologia (2012) 169:453–465 455

123

Statistical analyses

For each plot, we merged data of the four traps and for both

study years 2005 and 2006. We used the Bray–Curtis

coefficient (Bray and Curtis 1957) to calculate community

similarity of cavity-nesting hosts (bees and wasps) and of

their parasitoids among all plots within the same plant

diversity level. The Bray–Curtis coefficient is related to the

Sørensen index of similarity but is better suited for quan-

titative data because of its sensitivity to sample size. The

calculation was performed using the software Estimate S

(Version, Win 8.00). All further data analyses were per-

formed by using the statistical software R (R Development

Core Team, Vienna Austria. http://www.R-project.org.

Version 2.9.1, package base).

To test if community similarities differed between plant

diversity levels, we used a permutation test. We produced

random values of the Bray–Curtis index and calculated the

mean differences between the diversity levels based on

1,000 repetitions. We then compared the observed mean

difference between the diversity levels with the randomly

produced differences and noted how many times the

observed difference was either smaller than the random

difference (if the observed mean differences were negative)

or higher than the randomly produced ones (if the observed

mean differences were positive). The observed difference

between two diversity levels was considered to be signifi-

cant, if it differed from the randomly produced values less

than 50 times of the 1,000 repetitions (5% level).

To test if plant species composition and the composition

of the cavity-nesting hymenoptera community were cor-

related within plots,we produced two matrices. The first

matrix contained measures of the Euclidean distance

between all possible pairs of plots based on plant species

cover data (average of data of 2005 and 2006). The second

matrix consisted of pairwise Euclidean distances between

plots based on the abundance data of the cavity-nesting

host community. We tested for a correlation between the

matrices using Mantel tests implemented in the R package

ade4 (Dray and Dufour 2007).

We measured host diversity as the number of cavity-

nesting species (bees or wasps). The number of brood cells

per plot was defined as (brood cell) density of hosts (bees

and wasps). Rate of parasitism was calculated as the ratio

of the brood cell density of parasitoids over hosts.

We analysed the effect of vegetation on the cavity-

nesting community using a mixed effects model with type-I

sums of squares (Crawley 2002; Schmid et al. 2002). If

Q–Q plots showed deviations from normality (see

Tables 2, 3), we transformed the data (square-root, log or

arcsine square-root transformation). For bees and wasps,

we performed different models with different explanatory

variables, as both groups strongly differ in their diet.

Cavity-nesting bees strongly depend on flowers, because

adults and their larvae feed on pollen and nectar, and we

therefore included flower diversity and the percentage of

blossom cover (resource availability for bees) into the

analysis. In contrast, larvae of cavity-nesting wasps are

Table 1 List of found parasitoid species and their frequency of

occurrence

Parasitoid Host

bee

species

Host

wasp

species

Total

number of

host species

Number

of nests

attacked

Cacoxenus indagator 2 0 2 3

Chrysis cyanea 1 7 8 136

Chrysis ignita 0 3 3 6

Gasteruptionidae 5 2 7 85

Ichneumonidae 4 2 6 25

Lepidoptera larvae 2 0 2 3

Megatoma undata 2 2 4 8

Melittobia acasta 9 7 16 313

Omalus auratus 0 2 2 8

Sapyga quinquepunctata 1 0 1 7

Sapyga decemguttata 1 0 1 1

Stelis sp. 1 0 1 1

Trichodes apiarius 1 0 1 1

Table 2 Summary of overall effects on cavity-nesting bees and

wasps

Explainatory

variable

df F value

Bee

diversity

Brood

cell

density

beesb

Wasp

diversity

Brood

cell

density

waspsa

Brood cell density

host

1 75.8*** – 56.3*** –

Host diversity 1 – – – –

Block 3 1.12 1.01 0.196 7.70***

Edge 1 0.194 2.11 7.45** 6.30*

Blossom cover 1 0.552 0.981 – –

Plant dry weight 1 – – 0.976 1.42

Flower diversity 1 0.0222 6.81* – –

Plant diversitya 1 0.0760 1.12 1.94 0.325

Columns 3–10 show F values, for the response variables listed in the

first row. The first column shows the main factors tested in the

models, in the sequence in which they were fitted. Models always

started with a degree of freedom of 77, resulting from 78 plots. The

second column shows the degrees of freedom (df) for each of the

predictor variables

* P \ 0.05; ** P \ 0.01; *** P \ 0.001a Log-transformedb Square-root-transformedc Arcsine square-root-transformed in case of non-normal distribution

456 Oecologia (2012) 169:453–465

123

predators and only adults feed a little on pollen, and we

therefore added community biomass (plant productivity) as

additional explanatory variable into the models, as plant

productivity is known to increase insect abundance (food

resource for wasps) (Scherber et al. 2010). For analysing

overall effects on cavity-nesting bees, we fitted models

including the following explanatory variables: block (cat-

egorical), edge (categorical), blossom cover (numeric),

flower diversity (numeric) and plant diversity (numeric).

Accordingly, for analysing overall effects on cavity-nesting

wasps we included block, edge, plant productivity

(numeric) and plant diversity into the models. The factor

block (1–4) represents a gradient in abiotic conditions from

the river Saale. Plots assigned to block one are closest to

the river, whereas block four is furthest from the river. We

classified the factor edge as follows: 0 = within the

experimental field site without adjacent source habitat; 1 =

at the edge of the experimental field site with adjacent

source habitat or river bank (meadow or river). Blossom

cover is the mean percentage of plot area (20 9 20) in

bloom. Plant productivity is the mean plant productivity

(g/m2) of 2005 and 2006. For each year, we accumulated

the mean biomass (average of four/three samples per plot)

from peak standing biomass in May and August 2005 and

2006. Flower diversity is the merged number of flowering

plant species between May and August in 2005 and 2006.

In analysis of species richness data (diversity of wasps and

bees, diversity of parasitoids), we included the appropriate

abundance data (brood cell density of bees, wasps or par-

asitoids), to correct for changes in the brood cell density.

Those abundance data entered the model after the factors

block and edge. Analysis with parasitoid diversity as

response variable additionally contained the diversity of

their hosts as independent variable, after the factors block

and edge. Models where parasitism rate was the response

variable were completed by entering the diversity of hosts

or parasitoids, respectively, as independent variable after

the factors block and edge.

As an additional method, structural equation models

(Grace 2006; Pugesek et al. 2003) were used to show direct

and indirect effects of plant and flower diversity on cavity-

nesting bees and wasps, their natural enemies and ecosys-

tem functions at higher trophic level. The recommended

minimum sample size for using SEM is 200 (Arbuckle and

Wothke 1995; Pugesek et al. 2003; Grace 2006) and so the

results have to be seen as being exploratory (our sample

size, n = 78). Based on our hypothesis and according to

the mixed effects model we used for analyzing overall

effects of plant and flower diversity (see above), we con-

structed two different a priori models for cavity-nesting

bees and wasps, their natural enemies and parasitism rates

(see Online Resources 1 and 2 in Supplementary materi-

als). The initial model for cavity-nesting bees contained

beside plant diversity, the effect of edges and the block

design also flower diversity and blossom cover as possible

explanatory variables, to account for the impact of food

availability. Adults of cavity-nesting wasps only rarely

feed on pollen and larvae have a predatory diet. Therefore,

we included in addition to plant diversity, the effect of

edges and the block design plant productivity in the initial

model for cavity-nesting wasps. Both models included all

possible direct and indirect paths to higher trophic level.

Table 3 Summary of overall effects on parasitoid diversity and parasitism rate of cavity-nesting bees and wasps

Explainatory variable df F value

Bee parasitoid

diversityaParasitism

bees %cWasp parasitoid

diversity

Parasitism

wasps %c

Parasitoid diversity 1 – 79.2*** – 15.4***

Brood cell density hostsb 1 21.0*** 26.3*** 81.7*** 1.37

Host diversity 1 0.702 0.0194 14.9*** 7.67**

Block 3 0.284 0.258 2.69 2.13

Edge 1 0.284 0.398 0.0133 0.234

Blossom cover 1 0.0706 4.00 – –

Plant dry weight 1 – – 0.284 2.54

Flower diversity 1 1.34 0.228 – –

Plant diversitya 1 0.0341 2.15 1.454 1.02

Columns 3–10 show F values, for the response variables listed in the first row. The first column shows the main factors tested in the models, in

the sequence in which they were fitted

** P \ 0.01; *** P \ 0.001a Log-transformedb Square-root-transformedc Arcsine square-root-transformed in case of non-normal distribution

Oecologia (2012) 169:453–465 457

123

All subsets of our initial model were tested using maximum

likelihood estimation and models were simplified stepwise

until we reached a final model with the lowest AIC (Akaike

information criterion) score. For each model (initial and

final), we gave the number of distinct parameters being

estimated, Cmin (the minimum value of the discrepancy C),

AIC score and BCC (the Browne–Cudeck Criterion) (see

Online Resources 1 and 2 in supplementary materials).

SEMs were performed in Amos v.19.0 (IBM� SPSS�

Amos, http://www.spss.com/amos/).

Results

Cavity-nesting community structure and similarity

in response to plant diversity

Overall, 1,921 nests and 7,044 brood cells of 41 hymenoptera

host bee and wasp species where counted in the nesting traps

in 2005 and 2006 (see Online Resources 3 and 4 in Supple-

mentary materials for species names and abundances). Of the

41 host species, 22 species were bees (Apidae) and 19 species

were wasps: 10 digger wasp species (Sphecidae), 8 mason

wasps (Eumenidae), and 1 species of spider wasp (Pompil-

idae). Digger wasps were the most abundant family with

61.1% of all brood cells, followed by bees (35%), mason

wasps (3.5%), and spider wasps (0.4%). Thirteen species of

parasitoids attacked an average of 10.0% of brood cells

constructed by bees, 12.7% of the brood cells constructed by

digger wasps, 16.23% of brood cells constructed by mason

wasps, and 8.5% of brood cells constructed by spider wasps.

The most common parasitoid species was the gregarious

chalcid wasp Melittobia acasta, Walker, which attacked in

total 16 host species in 313 nests (Table 1).

The similarity in species composition of the host (bees

and wasps) communities was higher among the 16 species

mixtures plots than among plots in all the lower plant

diversity levels (Fig. 1a). Similarity in species composition

of the parasitoid communities also increased with

increasing plant diversity (Fig. 1b).

A comparison of similarity matrices of plant species

composition (mean plant species cover for 2005 and 2006)

and plant diversity showed a significant correlation

between plant cover data and plant diversity (Mantel test:

r = 0.19, simulated P value = 0.009). The comparison of

similarity matrices of plant species composition and host

(bees and wasps) abundance showed no significant corre-

lation between plant cover data and host abundances

(Mantel test: r = 0.12, simulated P value = 0.078).

Overall effects on cavity–nesting bees and wasps

and on host-parasitoid interactions

The diversity of bees was not affected by either plant

species richness, flower diversity or blossom cover

(Table 2; Fig. 2a), and increased with increasing brood cell

density of bees (Fig. 2b). Brood cell density of bees was

positively related to flower diversity (Table 2; Fig. 2c).

The diversity of bee parasitoids was not affected by either

plant diversity, flower diversity or blossom cover (Table 3;

Fig. 2d), and only increased with increasing brood cell

density of bees (Table 3). Furthermore, high brood cell

density of bees decreased parasitism rate for cavity-nesting

bees, whereas higher number of parasitoid species led to an

increase in parasitism (Table 3; Fig. 3a).

The diversity of wasps (host species) did not change

with changing plant diversity or plant productivity, and was

higher in plots at the edge than at the interior of the

a

Plant diversity1 2 4 8 16

Bra

y-C

urtis

Inde

x ho

sts

A

AA A

B

0.16

0.18

0.20

0.22

0.24

b

Plant diversity1 2 4 8 16B

ray-

Cur

tis In

dex

para

sito

ids

A

B

C

D

BC

0.2

0.3

0.4

0.5

Fig. 1 Effect of plant diversity on the similarity of a the host (bee

and wasp) community and b the parasitoid community among plots of

the same level of plant diversity. Significant differences in the

similarity of the host community exist between monocultures

(P = 0.002), 2-species mixtures (P = 0.047), 4-species mixtures

(P = 0.018), and 8-species mixtures (P = 0.007) versus 16-species

mixtures. Significant differences in the similarity of the parasitoid

community exist between monocultures and the 2-species mixtures

(P \ 0.001), 4-species mixtures (P = 0.005), 8-species mixtures

(P \ 0.001), and 16 -species mixtures (P \ 0.001). Two-species

mixtures differ from the 4- (P = 0.051) and 16-species mixtures

(P \ 0.001), and 4- (P \ 0.001) and 8-species mixtures (P \ 0.001)

differ from the 16-species mixtures. Black dots means ± standard

errors (SE). Significant differences between the plant diversity levels

are indicated by different capital letters above the black dots

458 Oecologia (2012) 169:453–465

123

experimental field site (averaged 3.4–2.5 species/plot)

(Table 2; Fig. 2a). Additionally, wasp diversity increased

with increasing brood cell density of wasps (Table 2;

Fig. 2b). Brood cell density of wasps was not affected by

plant diversity or plant productivity, and was higher in

plots at the edge than at the interior of the experimental

field site (averaged 88–31 brood cells/plot), and decreased

with increasing distance to the river (Table 2). The diver-

sity of wasp parasitoids did not change with increasing

plant diversity or plant productivity (Table 3; Fig. 2d).

Parasitoid diversity attacking cavity-nesting wasps was

shown to be caused by an increase in brood cell density and

diversity of cavity-nesting wasps (host species) (Table 3;

Fig. 3b). Further, wasp parasitoid diversity decreased with

increasing distance to the river (block effect; Table 3).

Parasitism of cavity-nesting wasps decreased with

increasing diversity of its hosts, and increased with the

diversity of its parasitoids (Table 3; Fig. 3c).

Direct and indirect effects on cavity-nesting bees

and wasps and on host–parasitoid interactions

The most parsimonious models of structural equation

models showed, that effects of plant diversity on cavity-

nesting bees and wasps were predominantly indirect effects

(Fig. 4a, b; Online Resources 1 and 2).

Brood cell density of cavity-nesting bees was indi-

rectly positively affected by plant diversity via increasing

flower diversity. The same could be explored for bee

diversity, which increased with increasing brood cell

density. Plant diversity also had an indirect positive effect

on the number of parasitoid species attacking cavity-

nesting bees via increased brood cell density which in

turn was positively influenced by increasing flower

diversity. Parasitism rate of cavity-nesting bees was

positively influenced by increasing parasitoid diversity

attacking bee (hosts). Additionally, increasing brood cell

density of bees led to a decrease in parasitism rate of

bees, yet there was no overall direct or indirect effect of

plant diversity on parasitism rate of bees. We could not

explore any indirect or direct effects of the blossom cover

of the plot.

Plant diversity had a direct positive effect on the

diversity of cavity-nesting wasps, but did not influence

their brood cell density, either directly or indirectly via

plant productivity.

The number of species attacking cavity-nesting wasps

(hosts) was indirectly positively affected by increasing

wasp diversity which in turn increased with increasing

plant diversity. There was no direct or indirect effect of

plant diversity on parasitism of cavity-nesting wasps, but

increasing numbers of species attacking wasps (hosts) led

to an increasing parasitism rate. Additionally, parasitism

rate decreased with increasing diversity of cavity-nesting

wasps. There was neither a direct nor an indirect effect of

plant productivity on cavity-nesting wasps, their parasit-

oids or parasitism rate, but a strong edge effect, as explored

already in the mixed effects models (Tables 2, 3).

a

Sown plant diversity1 2 4 8 16

Div

ersi

ty o

f hos

ts

1

2

3

4

5

6

7

bees

wasps

b

Brood cell density0 100 200 300

Div

ersi

ty

0

2

4

6

8bees, r²= 0.38

wasps, r²= 0.30

c

Flower diversity0 2 4 6 8 10 12B

rood

cel

l den

sity

of b

ees

0

20

40

60

80

d

Sown plant diversity1 2 4 8 16

Div

ersi

ty o

f par

asito

ids

1

2

3

4

bees

wasps

Fig. 2 Effects of a plant

diversity on the diversity of bees

and wasps, b brood cell density

of bees (solid line) and wasps

(dotted line) on the diversity of

bees and wasps, c of flower

diversity on brood cell density

of bees, and d plant diversity on

the diversity of parasitoids of

bees and wasps. In (a, d) blackdots means ± standard errors

(SE). In (b, c) each dot stands

for one plot. Black dots indicate

the relationship for bees and

white dots for wasps. For

statistics, see Table 2

Oecologia (2012) 169:453–465 459

123

Discussion

The main result of our study was that increasing plant

diversity of the plant community had direct and indirect

positive effects on the brood cell density and diversity of

cavity-nesting hosts (bees and wasps) and their parasitoids,

but no effect on the ecosystem function of the higher

trophic level (parasitism rates of hosts). Abundances and

diversity of wasps were also affected by the surroundings

of the experimental plots, indicating the importance of

controlling for these variables both by appropriate block-

ing, and by including them into the statistical analysis.

We found a high diversity of cavity nesting hosts, 41

species, which agrees with previous studies that have

described high diversity in extensively managed grasslands

(e.g. Kwaiser and Hendrix 2008; Moron et al. 2008). We

also found a surprisingly high number of bee species (22

bee species and 19 wasp species), while former studies of

cavity-nesting hymenoptera in Europe, in other habitat

types, found lower numbers and more wasp than bee spe-

cies (hosts) (Gathmann and Tscharntke 1999; Steffan-

Dewenter 2002; Albrecht et al. 2007; Holzschuh et al.

2009; Sobek et al. 2009; Schuepp et al. 2010). Bee brood

cell density was lower than wasp brood cell density and

this may be explained by the mowing event in June. During

that period, bees are not able to provision their nests with

pollen or nectar because of the absence of flowering plants

in the study plots and their need to travel longer distances

to provision their nests, while the food resource of wasps

(arthropods) is only disturbed, but not removed by mowing

events.

Effects of plant diversity on the similarity

of the cavity-nesting communities

Our results indicate that the similarity of the host com-

munity was lower in the low plant diversity plots (up to

eight species) than plots with 16 plant species. There was a

correlation between plant diversity and plant community

composition, but we could not detect a correlation between

plant species composition and host species composition

(see ‘‘Cavity-nesting community structure and similarity in

response to plant diversity’’, Mantel tests). Therefore, we

can assume that the higher similarity of host communities

in high diversity plots is not only due to a higher overlap in

plant species composition between plots but to a diversity

effect per se. The high diversity plots, although they dif-

fered in plant identity and composition, attracted similar

host species, suggesting functional redundancy within

diverse plant communities in terms of what they offer to

hosts. Higher similarity in host composition of diverse

plant communities could lead to increased similarity in

their functioning (predation for wasps or pollination for

bees).

Community similarity of the parasitoid communities

that attack bees and wasps followed the same patterns as

the host community, and was lower in the low plant

diversity plots (up to 8 species) than plots with 16 plant

species. As most of the parasitoid species found seem to be

oligophagous or even monophagous, except for a few

Brood cell density of bees

0 20 40 60 80

Par

asiti

sm r

ate

of b

ees

[%]

0

20

40

60

Wasp diversity (hosts)

1 2 3 4 5 6 7

Was

p pa

rasi

toid

div

ersi

ty

1

2

3

4

5

6

Wasp diversity (hosts)

1 2 3 4 5 6 7

Par

asiti

sm r

ate

of w

asps

[%]

0

20

40

60

80

100

a

b

c

Fig. 3 Effects of a brood cell density of bees on bee parasitism,

b wasp diversity on wasp parasitoid diversity, and c wasp diversity

(hosts) on wasp parasitism. Other conventions follow Fig. 2. Dots of

different plots can also be superimposed on each other. For statistics,

see Table 3

460 Oecologia (2012) 169:453–465

123

parasitoid species, which are highly polyphagous (such as

Melittobia acasta and Chrysis cyanea, L.; see also

Table 1), parasitoid identity is strongly influenced by the

host identity, hence explaining the related patterns. The

positive effect of plant diversity on the community simi-

larity of hosts and of their parasitoids also indicates that

high plant diversity can have a stabilising effect on the

identity of species in the community of the lower as well as

of the higher trophic levels. Our results contribute to the

long-standing diversity–stability debate (Pimm 1991;

Naeem and Li 1997; McCann 2000; Loreau et al. 2003;

Tilman et al. 2006), and underline the predicted positive

effect of plant diversity on the community stability (Elton

1958; Haddad et al. 2011).

Effects of plant diversity on cavity-nesting bees

and wasps

Changes in plant diversity are known to mediate changes in

flower diversity, community biomass, LAI, and vegetation

a

b

Fig. 4 Final, most

parsimonious structural

equation models relating plant

diversity and the diversity,

density and parasitism of cavity-

nesting a bees and b wasps.

Brood cell density of bees was

square-root transformed, brood

cell density of wasps and

parasitoid diversity of bees were

log-transformed. Parasitism

rates of bees and wasps were

arcsine square-root-

transformed. During model

simplification using maximum

likelihood estimation, single

paths were removed from the

original models (see Online

Resources 1 and 2 in

Supplementary materials). As a

final model, we selected the

models that had the lowest AIC

values. Standardised path

coefficients are given next to the

arrows with significances

indicated by *P \ 0.05,

**P \ 0.01, ***P \ 0.001.

Unexpected variance is denoted

by ‘e’. Detailed information

about the original and final

models (Cmin, AIC, BCC), and

about the strength of indirect

effects, are given in Online

Resources 1 and 2

Oecologia (2012) 169:453–465 461

123

height, which in turn affect arthropod abundance and

diversity (Hooper et al. 2005; Balvanera et al. 2006;

Marquard et al. 2009), and our results also showed a

positive relation between flower diversity and plant diver-

sity. Surprisingly, the proportion of flowering plant species

among all plant species was much lower for high diversity

plots than for low diversity plots. A possible explanation

for this pattern is the increasing possibility to have some

high biomass species in high diverse plots that shade all the

others.

Diversity of the bees (hosts) was indirectly positively

affected by plant diversity via increasing brood cell density

of bees, which in turn increased with increasing flower

diversity. Flower diversity increased with increasing plant

diversity. The direct effect of flower diversity on the

diversity of bees via increasing brood cell density is caused

by the feeding behaviour of the cavity-nesting bees. Bees

(adults and larvae) feed on pollen and nectar and therefore

directly depend on flower diversity. Surprisingly, the

blossom cover, which represents the amount of food

resources for bees, had no significant effect on the diversity

and density of cavity-nesting bees, indicating the impor-

tance of food quality instead of quantity. The positive

relationship between the brood cell density of bees on their

diversity provides support to the well-known relationship

of sample size and species richness (in support of the more

individual hypothesis).

The increase in wasp diversity (host) arose directly from

an increase in plant diversity. The plant diversity effect was

not very strong and was only found by using structural

equation models. According, the patterns we found for bees

(hosts) increasing brood cell density of wasps (hosts) led to

higher wasp diversity, supporting the more individual

hypothesis (see above). Wasp diversity was strongly

affected by the surrounding habitat: higher brood cell

density and diversity of wasps occurred in plots at the edge

of the experimental field site. These edge plots were con-

nected to potential source habitat for wasps (meadow or

river bank, woody habitats). Previous studies have shown

that wasps find highest prey abundances in woody habitats

as found at the edges of our experimental field site, and, if

available, prefer these woody habitats in comparison to

open grassland habitats (Schuepp et al. 2010).

Previous studies on the effect of biodiversity on cavity-

nesting hymenoptera gave mixed results; only a few studies

found positive effects of plant diversity on cavity-nesting

hymenoptera (Steffan-Dewenter and Leschke 2003; Klein

et al. 2004; Albrecht et al. 2007; Sobek et al. 2009), while

others reported no relationship between the hymenoptera

host community and plant diversity (Tscharntke et al. 1998;

Sheffield et al. 2008). Such diverging results may have

been caused by the fact that gradients in plant diversity in

these studies were a result of changes in management or

land-use intensity with associated changes in plant com-

munity composition that also themselves affected the

community of cavity-nesters. In our experimental study,

we directly manipulated plant diversity. Strong effects of

plant diversity on the insect community were also found in

earlier experimental biodiversity studies (e.g. Knops et al.

1999; Haddad et al. 2001, 2009; Petermann et al. 2010;

Scherber et al. 2010), and the positive effect on the

diversity of bees and wasps in our study may be explained

by increasing resource heterogeneity (bees: pollen and

nectar; wasps: arthropods), which increases attractiveness

for insect species seeking single and multiple resources

(Tscharntke et al. 1998; Potts et al. 2003; Ghazoul 2006).

Differences between bees and wasps may be caused by

the different role of adjacent habitats (meadow or river

bank, woody habitats) as foraging sites. Bees may pre-

dominantly find their food resources in open habitats (in

our study, the experimental grassland plots) and to find the

most attractive flower patches (high flower diversity),

whereas wasps may find highest prey abundances in the

adjacent habitats. For the most common wasp observed in

our study (Trypoxylon figulus), Schuepp et al. (2010) found

that brood cells built at forest edges, where wasps have the

choice between prey of open land and woody habitats,

contained predominantly prey species (spiders) living in

woody habitats. These results may explain the strong

benefit of edges for cavity-nesting wasps in contrast to

cavity-nesting bees.

Effects of plant diversity on parasitoids and parasitism

rates

The diversity of parasitoids attacking both host guilds (bees

and wasps) was indirectly affected by plant diversity via

the density (for bees) or diversity (for wasps) of their hosts.

Further, increasing host density (for bees) and diversity (for

wasps) led to lower parasitism rates, whereas higher

diversity of their respective parasitoids led to an increase of

parasitism.

The strong positive effects of brood cell density of bees

on the diversity of their parasitoids support the more

individual hypothesis (Srivastava and Lawton 1998). For

wasps, different mechanisms account for the patterns

found. Enhanced diversity of the wasps’ parasitoids arose

from increasing wasps diversity (hosts), which increased

with increasing plant diversity, supporting the resource

heterogeneity hypothesis (Hutchinson 1959; Southwood

et al. 1979). Thus, these results indicate the benefit of the

consumer level (parasitoid diversity) from the resource

diversity of the lower trophic level (host diversity). Our

results are in accordance with some other experimental

studies, focussing on other invertebrate taxa. For example,

Petermann et al. (2010) found indirect effects on the third

462 Oecologia (2012) 169:453–465

123

trophic levels (parasitoids) mediated by changes of the host

community (aphids) and no direct effects of plant diversity

on the highest trophic level. Another study of Knops et al.

(1999) found indirect effects of plant diversity on the

diversity and abundance of predators or parasites, mediated

by richness and abundance of the respective lower trophic

level (herbivores or predators). Other studies in abandoned

and managed coffee agroforestry systems on cavity-nesting

hymenoptera found effects of similar strengths on hosts and

their parasitoids. For example, Veddeler et al. (2010) and

Tylianakis et al. (2006) found that a diverse cavity-nesting

host community increased parasitoid diversity. The

observed patterns were explained by the increasing

resource heterogeneity of the host diversity (lower trophic

level), leading to corresponding changes at the higher

trophic level (parasitoid diversity), which may be explained

by the high specialisation of the parasitoid community and

a lack of intra-guild predation. In our study, the gregarious

wasp species Melittobia acasta attacked 16 host species,

but all other natural enemies (except Chrysis cyanea and 2

undetermined species which attacked 8, 6, and 7 species,

respectively) in our study attacked only 1–4 host species

(see Online Resources 3 and 4; Table 1). Thus, the

majority of parasitoid species in our study are very spec-

ialised in their resource use (larvae of host species or their

food) and therefore benefit from resource heterogeneity of

their hosts.

We showed a strong positive effect of parasitoid diver-

sity attacking bees and wasps (hosts) on parasitism rates of

bees and wasps. Those results of a positive relationship

between parasitoid diversity and parasitism support find-

ings of a positive diversity–function relationship in other

multitrophic systems (e.g. Cardinale et al. 2003; Gamfeldt

et al. 2005; Ives et al. 2005; see Tylianakis et al. 2006 for

underlying mechanisms). Further, a high diversity of wasps

and a high brood cell density of bees decreased parasitism

by their parasitoid communities. Similar results were found

in former landscape studies (Tylianakis et al. 2006; Ved-

deler et al. 2010) and in a meta-analysis of consumer-

resource experiments (Hillebrand and Cardinale 2004). The

mechanisms behind these patterns are speculative. Hille-

brand and Cardinale (2004) explained their consistent

results by an increased possibility to have unpalatable

species in a diverse host community, which reduces the

chance of the consumer to find their attractive hosts.

Another possibility for interpretation is a positive host

interaction, whereas a diverse and dense host community

can offer a more effective protection against parasitoids

(e.g. by patrol, by confusing) (Goodell 2003). The decrease

in parasitism rate of bees arising from increasing brood cell

density may also have been caused by egg limitation of the

parasitoid species (Heimpel and Rosenheim 1998). In

detail, the ratio of bee to parasitoid density increases with

increasing plant diversity, leading to a dilution effect

(Thies et al. 2008) and lower parasitism rates at high

diverse plots. Overall, there was no significant direct or

indirect effect of plant diversity on the parasitism rates of

cavity-nesting bees and wasps, and we therefore conclude

that the positive effect of enhanced parasitoid diversity and

the negative effect of the increased host density on para-

sitism rate may have neutralised each other.

In conclusion, the exposure of standardised nesting

resources along a plant diversity gradient showed that

diversity, brood cell density, and community similarity of

cavity-nesting bees, wasps and their parasitoids were neg-

atively affected by decreasing plant diversity. Our results

suggest that even small-scale plant diversity losses have a

number of concomitant effects on multitrophic interactions,

for example losses in community dissimilarity. By using

SEM, we elucidated underlying mechanisms of plant

diversity on higher trophic levels, with direct effects of

plant diversity on wasp diversity, but indirect on bee

diversity (via flower diversity and brood-cell density).

Open questions include the potential role of competitive

effects among flower visitors with increasing diversity,

changes in the behavior of bees and wasps leading to the

decreased rates of parasitism (Goodell 2003) and landscape

level effects.

Acknowledgments We acknowledge E.D. Schulze and B. Schmid

for helping to establish ‘‘The Jena Experiment’’. For the provision of

plant biomass and plant cover data, we greatly thank A. Weigelt and

E. Marquard. Further, we thank all people helping with the man-

agement of ‘‘The Jena Experiment’’, especially A. Weigelt as field

coordinator and the gardeners, S. Eismann, S. Hengelhaupt, S. Jun-

ghans, U. Kober, K. Kunze, G. Kratzsch, H. Scheffler, and U. Weh-

meier. The help during fieldwork by S. Creutzburg, M. Knauer and H.

Baldeweg and all the helpers during the weeding campaigns is greatly

acknowledged. ‘‘The Jena Experiment’’ is funded by the Deutsche

Forschungsgemeinschaft (DFG, FOR 456), with additional support

from the Friedrich Schiller University of Jena and the Max Planck

Society.

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