Journal of Animal Ecology 2012

doi: 10.1111/j.1365-2656.2012.01951.x

Complexity of multitrophic interactions in a grassland ecosystem depends on plant species diversity

Michael Rzanny* and Winfried Voigt
Institute of Ecology, Friedrich Schiller University, 07743 Jena, Germany

Summary 1. We studied the theoretical prediction that a loss of plant species richness has a strong impact on community interactions among all trophic levels and tested whether decreased plant species diversity results in a less complex structure and reduced interactions in ecological networks. 2. Using plant species-specic biomass and arthropod abundance data from experimental grassland plots (Jena Experiment), we constructed multitrophic functional group interaction webs to compare communities based on 4 and 16 plant species. 427 insect and spider species were classied into 13 functional groups. These functional groups represent the nodes of ecological networks. Direct and indirect interactions among them were assessed using partial Mantel tests. Interaction web complexity was quantied using three measures of network structure: connectance, interaction diversity and interaction strength. 3. Compared with high plant diversity plots, interaction webs based on low plant diversity plots showed reduced complexity in terms of total connectance, interaction diversity and mean interaction strength. Plant diversity effects obviously cascade up the food web and modify interactions across all trophic levels. The strongest effects occurred in interactions between adjacent trophic levels (i.e. predominantly trophic interactions), while signicant interactions among plant and carnivore functional groups, as well as horizontal interactions (i.e. interactions between functional groups of the same trophic level), showed rather inconsistent responses and were generally rarer. 4. Reduced interaction diversity has the potential to decrease and destabilize ecosystem processes. Therefore, we conclude that the loss of basal producer species leads to more simple structured, less and more loosely connected species assemblages, which in turn are very likely to decrease ecosystem functioning, community robustness and tolerance to disturbance. Our results suggest that the functioning of the entire ecological community is critically linked to the diversity of its component plants species. Key-words: arthropods, connectance, experimental grasslands, food webs, functional groups, interaction webs, invertebrates, partial Mantel test

Introduction
Anthropogenic changes to habitats and global climate confront ecosystems with an unprecedented loss of biodiversity (Pimm et al. 1995; Thomas et al. 2004). Plants are at the base of terrestrial food webs and additionally act as a physical microhabitat for most arthropod species, hence bottom-up effects through the trophic system are considered to be very strong (Price 2002; Schmitz 2010). Changes in plant diversity have also been shown to have a strong effect on the diversity of consumers (e.g. Haddad et al. 2009; Scherber et al. 2010). The extinction of basal species, such as plants, tends to increase the risk of secondary species extinctions (Koh et al. 2004; Dunne & Williams 2009). This loss cascades up to higher trophic levels where it may provoke changes in food bault & Loreau 2006; web structure and properties (e.g. The Haddad et al. 2009; Scherber et al. 2010). In particular, it has been suggested that highly connected communities tend to be more robust to secondary species loss (Dunne, Williams & Martinez 2002, 2004). A food web represents a network of complex trophic links among the members of an ecological community and allows researchers to improve the understanding of dynamics and interactive mechanisms of community processes (Pimm, Lawton & Cohen 1991). However, consumerresource interactions represent only one type of possible interactions among species. Species interact in multifaceted ways (e.g.

*Correspondence author. E-mail: michael.rzanny@uni-jena.de

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society

2 M. Rzanny & W. Voigt mutualism, facilitation effects, resource transforming, zoochory, supply of breeding places, habitat modication), and any attempts to depict realistic interactions among community members should not ignore non-trophic interactions (Price 2002; Berlow et al. 2004; Olff et al. 2009). To understand the dynamics and the interactive mechanisms of community processes, it is necessary to extend the focus from food web studies to the analysis of interaction webs (Goudard & Loreau 2008; Ings et al. 2009; Olff et al. 2009). Interactions between species have been shown to be very susceptible to environmental changes and to affect all ecosystem attributes from primary productivity to population dynamics (Suttle, Thomsen & Power 2007; Tylianakis, Tscharntke & Lewis 2007). But only recently have researchers begun to focus on interaction diversity as a response variable and relate it to various kinds of ecosystem changes (Albrecht et al. 2007; Tylianakis et al. 2008; Dyer et al. 2010). Yet direct effects of plant species diversity have been rarely related to changes in interaction diversity (Petermann et al. 2010; Ebeling, Klein & Tscharntke 2011). In practice, it is virtually impossible to observe the various kinds of interactions among species in a multitrophic community, directly and simultaneously. Species are embedded in complex interaction networks, and their individual response to environmental changes is always context dependent (Tscharntke et al. 2005; Wardle & Zackrisson 2005; Gundale, Wardle & Nilsson 2010), making individual species responses unpredictable (Ives & Cardinale 2004). Here we adopt a whole ecosystem approach and represent ecological communities as networks of interacting functional groups (Bengtsson 1998; Hulot et al. 2000; Berg et al. 2010; Siepielski et al. 2010). These networks show the dominant ecological relationships and provide a useful generalization to enable comparisons to be made between different ecosystems or stages independently of species identity (Voigt, Perner & Jones 2007). Their aggregated nature makes them less sensitive to local temporal and spatial changes (Berg & Bengtsson 2007). We dene functional groups as a group of species with a similar set of traits, which play an equivalent role in the ecological community (Cummins 1974; Blondel 2003). Interactions between functional groups have been inferred from partial Mantel correlations, calculated from abundances of functional group members on corresponding plots. Species are grouped based on similarity of functional characteristics assuming functional redundancy among functionally similar species. In this study, we present and compare functional group interaction webs based on replicated experimental plant communities of differing plant species richness. Our objectives were as follows: (i) to dene arthropod functional groups in an objective and reproducible manner and to construct interaction webs of functional groups to depict the dominating interactions, structuring ecological communities; (ii) to compare the functional group interaction patterns for experimental low plant diversity mixtures (four-plant species) and high plant diversity mixtures (16 plant species) in two different sampling years; and (iii) to test whether potential differences in the interaction strengths (IS) between functional groups are related to the number of species within these groups. Theory predicts that interaction web connectance will increase with species richness (Goudard & Loreau 2008). Accordingly, we expected that more diverse plant communities would also support more strongly connected and more complex interaction webs. To this end, we measure web complexity in terms of connectance, interaction diversity and mean IS for the whole community and, separately, for bidirectional functional group interactions of different trophic levels.

Materials and methods

EXPERIMENTAL DESIGN JENA EXPERIMENT

All data were collected between May and October 2003 and 2005 on 32 grassland plots of the Jena Experiment. These plots are 20 20 m in size and were established in spring 2002 (Roscher et al. 2004). The plots are located in the oodplain of the river Saale (altitude 130m a.s.l.) at the northern edge of Jena, Thuringia, Germany. The target plant communities with different species richness were established as random mixtures from seeds out of a pool of 60 species typically occurring in semi-natural, mesophilic grasslands in the surrounding region. To maintain the target plant species composition, all plots were manually weeded and mown twice a year in June and September, and they remained unfertilized throughout the experiment. 4-, 16- and 60-plant species mixtures were used for the analysis. All plant species were a priori assigned to four functional groups: grasses (16 species), legumes (12 species), tall herbs (20 species) and small herbs (12 species) based on the results of a cluster analysis involving morphological, phenological and physiological traits (see Roscher et al. 2004 for details). Arthropods were sampled on 16 plots of the 4-species mixtures (low plant diversity) and on the 14 plots of the 16-species mixtures. To provide comparable sample numbers, two 60-species mixtures were added to the group of 16-species mixtures (high diversity). Omitting (randomly) two 4-species mixtures and with them the 60-species mixtures did not change the general outcomes but decreased the number of signicant interaction for both species richness levels attributed to a lower sample size.

PLANT SAMPLING METHODS

In 2003, above-ground biomass was harvested once between 26 May and 6 June and again between 25 August and 5 September. In 2005, above-ground biomass was harvested once between 30 May and 8 June and again between 22 and 31 August. A 20 50 cm frame was placed on four predened positions in each plot, and all plants within this frame were cut to about 3 cm above-ground. Biomass was sorted to species level and dried at 70 C for 48 h, and the mean dry weight in g m)2 of each species of the four samples was taken as a measure for plant species biomass in each plot (Roscher et al. 2004).

ARTHROPOD SAMPLING METHODS

Arthropod abundance was estimated using two different techniques. Ground-associated arthropods were collected using two pitfall traps installed on each plot. They were emptied every three weeks (six times) during the growing period. Only during the mowing periods were the traps closed for about two weeks. Vegetation-associated arthropods were collected on ve randomly chosen subplots in the

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Plant diversity and multitrophic interactions 3

core area of each plot using an electric suction sampler (Brook et al. 2008) in combination with a biocenometer (bottomless, cube-shaped covering of gauze) covering an area of 075 075 m. Samples were taken ve times per year from May to October. The following taxa were sampled in 2003 and again in 2005: Diptera, Hymenoptera, Coleoptera, Araneae, Opiliones, Heteroptera and Auchenorrhyncha. Orthoptera were not found in 2003, so only data for 2005 were available, and Thysanoptera were sampled only in 2003. All the taxa listed above represent the main component of above-ground invertebrate diversity. The arthropods were mostly identied to species level, except for individuals from several terebrant Hymenoptera superfamilies, which in most cases were identied to the level of family or subfamily. Only taxa with at least ten sampled individuals in the whole experimental site were included in the analysis. nominal variables (Pavoine et al. 2009, see Table 1). All traits were weighted equally.

CLASSIFICATION OF ARTHROPOD FUNCTIONAL GROUPS

ARTHROPOD TRAITS

It is unlikely that a universal functional classication exists that is equally suitable for different purposes (Wright et al. 2006), so that the traits used for functional groupings always depend on the scope of the study (Petchey & Gaston 2006). A trait is considered functional if it affects tness directly or indirectly via its effects on growth, reproduction and survival (Violle et al. 2007). A fundamental distinction of functional traits separates effect traits and response traits (Lavorel & Garnier 2002; Naeem & Wright 2003; Laliberte et al. 2010). Response traits are associated with the response of species to environmental changes while effect traits determine their effect on ecosystem functions. For the classication of functional groups, only effect traits were considered, as only they are important in modifying community interactions. Traits that usually control resource use and feeding relationships are likely to have profound effects on ecosystem processes (Chapin et al. 1997; Bremner 2008). Knowledge on detailed functional traits for grassland arthropods is limited, and general conventions on selecting and coding functional traits for different arthropod taxa have not yet been developed. For this study, we selected traits that reect functional differences among species across very distinct phylogenetic groups. Therefore, the selected functional traits are expected to be generally applicable for all species of the multitaxon community. We intended to scale up the community to a number of interacting functional groups. Traits related to feeding play an important role, because the majority of vertical interactions are in fact trophic relationships. However, the inclusion of additional traits is necessary to take non-trophic effects into account (Bengtsson 1998). Because of this, we selected ten functional traits that were mainly related to different feeding strategies, but we also considered microhabitat distributions and life-history strategies (see Table 1). For species that shift feeding strategy (Diptera, Hymenoptera, Coleoptera) during their live history, we considered larval traits only because this stage is usually the feeding stage and so is more important in terms of abundance and biomass for ecosystem processes. Consequently, only species with terrestrial larvae were included. For the estimation of aerial mobility, the life stage with the highest aerial capabilities was decisive. Trait data were compiled from extensive literature searches. These traits were coded as variables of different statistical types (Table 1). Body mass was estimated from the mean length using published allometric equations (Rogers, Buschbom & Watson 1977) and were logtransformed prior to analysis. Trophic level and vertical distribution were fuzzy coded to adequately describe gradual differences and simultaneous occurrences of variable attributes. The remaining traits were coded as ordinal, nominal, dichotomous or binary multichoice

Because the variables describing functional traits are of various statistical types, we used a generalization of Gowers dissimilarity index to describe functional differences among species. Here we followed the approach of Pavoine et al. (2009). The resulting distance matrix was hierarchically clustered using Wards method, and the cut-off level of the resulting cluster tree was determined using mean silhouette width (Rousseeuw 1987). Mean silhouette width was calculated for different numbers of clusters, and the clustering tree was pruned when the subdivision to more clusters did not result in a substantial increase in this value. The resulting silhouette plot was inspected, and species with negative values (equates to misclassied samples) were assigned to their neighbouring cluster. Each cluster was then regarded as a functional group. The correlative relationships between the traits and the resulting functional groups were explored using non-metric multidimensional scaling (NMDS) (Clarke 1993).

DATA ANALYSIS

Arthropod abundance data were summed for each species on every plot over all sampling dates. Plant biomass was calculated as the mean of the four subsamples taken from each plot and was summed over both harvests. All data were log-transformed to improve statistical normality. Each functional group is represented as a matrix of s species and p plots (Fig. 1). In the rst step, MorisitaHorn dissimilarity was calculated for each plant and consumer functional group across all plots with the same plant species richness. The Morisita Horn dissimilarity index is superior to other such indices because it is negligibly inuenced by sample size and species richness (Magurran 2004). In the following step, these dissimilarity matrices were analysed using partial Mantel tests (Mantel 1967; Smouse, Long & Sokal 1986) (Fig. 1). Recent analyses using partial Mantel tests have produced new insights into complex ecological questions (Perner & Voigt 2007; Cushman & Landguth 2010; Maestre et al. 2010; Beaudrot & Marshall 2011), especially if other methods were not applicable. Structural equation modelling (Grace 2006), a powerful concept to study networks, is not useful if sample size is too small and, as in our study, the direction of relationships cannot always be determined unequivocally, that is, an essential assumption of structural equation models is not met. While a simple Mantel correlation, for example, between plant and consumer functional groups, indicates that similar plant communities support similar herbivore communities or, conversely, dissimilar plant communities support dissimilar herbivore communities, it remains unclear whether this relationship is direct or indirect, mediated through other biotic or abiotic factors. Partial Mantel tests, however, calculate the direct or pure relationship between two matrices by controlling for the effect of all the other (known and measured) descriptor variables and so, as in path analysis, allow causal inference. In principle, such relationships may emerge from (i) direct or indirect biotic interactions, (ii) a similar response to environmental conditions or (iii) by chance. Indirect biotic effects are relationships mediated by other functional groups of the same or a different trophic level(s). As environmental conditions are largely equal across the plots (randomized block design, but the block effect is negligible), and a permutation test is used to judge the statistical signicance of the partial Mantel correlation, signicant correlations between the

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4 M. Rzanny & W. Voigt

Table 1. List of species traits used for the classication of functional groups. All traits were compiled from literature. Data type coding follows Pavoine et al. (2009): quantitative (Q), fuzzy coded (F), binary multichoice (B), nominal (N), dichotomous (D) and ordinal (O) Data type Q F Trait Body mass Trophic level Attributes Unit range of values mg 04 04 04 04 04 04 01 01 01 01 01 01 01 01 01 01 01 01 01 Sucking chewing Endophytic endoparasitic exophagous 01 0 1 2 3 % Missing values 000 000 000 000 001 003 002 000 000 000 000 000 001 000 005 000 000 000 000 000 000 005

Vertical distribution

Feeding hunting strategy

h N N Mouthparts Exposition

Herbivorous Carnivorous Detritivorous Vegetation Ground Soil Dung Micro-organisms Dead plant material Fungi Carrion Stem Root Leaf Flower Flower products Seeds Pursue Sit and wait

D O

Parasitism Aerial mobility

Degree of omnivory

Degree of specialization

Static Passive At least some individuals y actively Active ying as most important mode of move One trophic level Two trophic levels Three trophic levels Monophagous Oligophagous Polyphagous

000 001

1 2 3 1 2 3

000

005

functional group distances are most likely caused by biotic interactions. A potential association between two distance matrices is necessarily mediated via the net effect of the manifold types of interactions between the members of the two functional groups. Therefore, we interpret a signicant partial Mantel correlation between two functional groups as a link between nodes (functional groups) of an interaction network and use the magnitude of the partial Mantel correlation as a measure of IS. Because we entirely used the same resemblance measure (MorisitaHorn dissimilarity), our hypothesis is that the resemblance patterns of two functional group matrices are correlated only positively or not at all. Thus, a one-tailed permutation test was used to estimate statistical signicance. We selected P < 005 as the threshold value. A link between two functional groups existed whenever rM was signicant. The value of rM is interpreted as a measure of IS between two functional groups. Partial Mantel tests were calculated in turn for all pairs of functional groups from different trophic levels (vertical interactions, i.e. producerherbivore, producercarnivore, and herbivorecarnivore) and from the same trophic level, respectively (horizontal interactions, i.e. herbivoreherbivore, carnivorecarnivore). Note that in the context of horizontal interactions, we treated herbivores and detritivores

as being on one and the same trophic level (herbivores). Consequently, links between herbivores and detritivores and between the two detritivorous functional groups also contribute to herbivoreherbivore connectance. This was necessary because there were only two detritivorous functional groups (see results), and owing to the low number of potential interactions, these values would hardly be comparable to the others. In the case of vertical interactions, the effect of all functional groups from the third trophic level was amalgamated in a compound distance matrix and was partialled out. In the case of horizontal interactions, the effects of the two remaining trophic levels were partialled out. In a nal step, interaction webs were derived from all signicant partial Mantel correlations by linking all associated functional groups with a line. Line width increases quadratically with the value of rM. Interaction webs were plotted for both high and low plant diversity plots and for both sampling years.

QUANTIFYING INTERACTION WEB STRUCTURE

In recent years, a great variety of network indices have been developed to describe structural attributes of interaction networks

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Plant diversity and multitrophic interactions 5

Correlated functional groups FG2 FG1

SP1 SP2 SPx PT1 . . . PT2 . . . PTx . . . M-H Dissimilarity SP1 SP2 SPx PT1 . . . PT2 . . . PTx . . . M-H Dissimilarity

One or two matrices for statistical control Controlling trophic level 1

M-H Dissimilarity SP1 SP2 SPx PT1 . . . PT2 . . . PTx . . .

Permutation test

Partial Mantel test

Fig. 1. Diagrammatic summary of the different steps of analysis performed. Matrices in brackets represent species abundance matrices, and triangles represent distance matrices. SP, Species; PT, plot; M-H, MorisitaHorn.

Controlling trophic level 2

M-H Dissimilarity SP1 SP2 SPx PT1 . . . PT2 . . . PTx . . .

Partial Mantel correlation rM

(Dormann et al. 2009; Bluethgen 2010). The functional group interaction networks we develop here are (i) comprised of an equal number of nodes, (ii) connected through undirected links, (iii) relatively small compared with many species-based interaction networks and (iv) many of the network indices are strongly correlated. These properties rule out many of these indices and so we restricted our analysis to the three most basic and universally adopted network indices describing structural network properties: connectance, interaction diversity and mean IS. These indices are predicted to impact community stability and ecosystem functioning (Tylianakis et al. 2010) and have been shown to be sensitive to various perturbations in speciesbased interaction networks (e.g.: Albrecht et al. 2007; Ebeling, Klein & Tscharntke 2011). Interaction diversity and connectance are inherently correlated, as all networks are comprised of the same nodes. We have still reported results for both indices here to enable comparisons with other studies. Connectance (CFG) was calculated as the number of realised interactions between specied trophic levels (L) divided by the number of potential interactions (LMax). CFG L=LMax Interaction diversity (ID) was calculated using the Shannon index: ID
n X i0

therefore implies a strong degree of spatial coupling among their component species and in turn indicates strong mutual dynamics between them. Altogether, they can be interpreted as different aspects of ecosystem complexity with connectance and interaction diversity, referring to the diversity of interactions among different functional groups, and IS, referring to the state of a particular interaction between two functional groups. These indices were calculated for all pairs of trophic levels (producer herbivore, producer carnivore, herbivore carnivore; vertical interactions), all pairs within trophic level (herbivoreherbivore, carnivorecarnivore; horizontal interactions) and for the whole interaction web. To exclude the possibility that the differences in interaction patterns are sensitive to the chosen threshold alpha level, we increased this level to P < 01 and recalculated the interaction webs. All statistical analyses were performed using the statistical software R 2.12.0 (R Development Core Team 2010) using the packages vegan (Oksanen et al. 2010), ade4 (Dray & Dufour 2007), ecodist (Goslee & Urban 2007) cluster (Maechler et al. 2005) and diagram (Soetaert 2009).

pi log2 pi

Results
FUNCTIONAL GROUP IDENTIFICATION

where pi is the proportion of interaction i to the total sum of n observed interactions, that is, each partial Mantel correlation was divided by the total sum of all signicant partial Mantel correlations. Mean IS is the arithmetic mean of all signicant interactions. IS
n 1X pi n i0

It is important to note that in webs of aggregated functional groups, single-species interactions add up to functional group interactions. Hence, the interpretation of functional groups IS differs from IS in species-based webs. The number of functional groups in the interaction webs is constant, while the number of species within functional groups may change. The effects of both a few strong and many weak species interactions are additive and may jointly increase mean functional group IS. High IS between two functional groups

In total, 60 plant species and 427 arthropod taxa (2003: 325 arthropod taxa with 67 095 sampled individuals; 2005: 322 arthropod taxa with 56 652 individuals) were considered for the classication of functional groups (Table S1). In the resulting distance matrix, most traits contributed similarly to the global distance, while the contributions of body mass and degree of omnivory were underrepresented (Appendix S1) and thus are less indicative for group separation. Cluster analysis of the distance matrix resulted in a well-separated dendrogram and evaluation of the mean silhouettes revealed 13 clusters as a statistically justied cutting level (Appendix S2). A following NMDS (three dimensions, nal minimum

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology

6 M. Rzanny & W. Voigt stress = 011) indicates a strong separation of herbivorous and carnivorous species along the rst axis and a separation of species with sucking and chewing mouthparts along the second axis (Fig. 2). The third axis again separates the different trophic levels. The clusters were interpreted as functional groups and named according to their most characteristic traits through thorough exploration of the NMDS plot in combination with the tted trait variables (Fig. 2, Table 2). The functional classication reects a basal trophic community organization in herbivorous, detritivorous and carnivorous functional groups (Fig. 2.). The plant functional groups had been dened earlier (see Roscher et al. 2004), and this classication was directly adopted in our interaction webs.

HERBIVORES

Five functional groups were considered as herbivorous. Plant suckers (HSU) are often quite mobile and mostly inhabit the

Axis 2

Aerial mobility
6 8 11 7

Distribution ground
9 10

Endophytic

13 2

Carnivory

Degree of specialisaon

12 3

Herbivory

Distribution vegetaon
1

Sucking

Axis 1

Axis 3

Carnivory

Distribution vegetation

Endoparasitic

9 3 4 1 Sucking 5 10

12

Aerial mobility

11 67 2 13

Herbivory Degree of omnivory Distribution soil

Detritivory

Axis 2

Fig. 2. Non-metric multidimensional scaling ordination plot based on Gowers distance among arthropod species. Numbers in the centre of each ellipse represent group means. Arrows represent most important standardized tted trait variables (ordinal fuzzy). Cross symbols represent cendroids of most important tted nominal trait variables.

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Plant diversity and multitrophic interactions 7

Table 2. Functional groups and the number of arthropod taxa collected on the experimental plots Trophic level Plants Code PSH PGR PTH PLG HSU HSP HRF HSC HEP CPO CVS CGC CWS CGS OMG DES DSS Functional group Small herbs Grasses Tall herbs Legumes Plant suckers Seed predators Root feeders Specialized chewers Endophytics Parasitic species Vegetation-associated suckers Ground-living chewers Web spiders Ground-living suckers Omnivores Endophytic saprophages Soil-living saprophages Important taxa Misc. Poaceae Misc. Fabaceae Auchenorrhyncha, Heteroptera Carabidae Coleoptera Coleoptera Diptera, Hymenoptera, Diptera Diptera Carabidae, Staphylinidae Araneae Araneae Misc. Diptera Diptera, Coleoptera Number of taxa 12 16 20 12 59 34 18 32 35 45 16 40 34 31 34 10 39

Herbivores

Carnivores

Detritivores

vegetation layer. The larvae of endophytics (HEP) live within the above-ground parts of plants as miners or stem borers. They feed almost exclusively mono- or oligophagously. Specialized plant chewers (HSC) are also mostly mono- or oligophagous. They have chewing mouthparts and inhabit the vegetation layer. Larvae of the root feeders (HRF) are part of the below-ground soil fauna and feed on the roots of several plant species. Seed predators (HSP) feed on a mixed diet of plant seeds and, in most cases, additionally on small arthropods. They are rather large species compared with the members of other functional groups and are able to y actively.

(CGC) comprise polyphagous Carabidae, Staphylinidae and Diptera. Web spiders (CWS) weave webs of different shapes and types. Vegetation-associated suckers (CVS) are oligophagous carnivores, searching for prey in dense vegetation. A number of Diptera and Coleoptera species belong to this group. The last group is formed by large ground-living, sucking arthropods (CGS). This is again a polyphagous group predominantly constituted by ground-living spiders.

FUNCTIONAL GROUP INTERACTIONS

DETRITIVORES

Two functional groups mainly showed detritivorous feeding habits. The endophytic saprophages (DES) are saprophytophagous and mine inside decomposing stems and leaves. The adults are strong and active iers. In contrast, soil-living saprophages (DSS) are exclusively saprophagous and feed on rotten plant material, dung, fungi or carrion. Species of this group belong to the orders Diptera or Coleoptera and live predominantly in the soil or on the ground.

CARNIVORES

Six functional groups were considered as carnivores. The omnivores (OMG) are ground-living and polyphagous chewing species. All are carnivorous but they additionally pursue at least one further feeding strategy (herbivorous or detritivorous) and are usually capable of active ight. The remaining groups are exclusively carnivorous, with parasitic species (CPO) representing a group of species which is consistently specialized on particular host species. Most of them are endoparasites and nearly all are active and strong iers searching for prey within the vegetation layer. Ground-living chewers

Species richness of some functional groups differed signicantly between the low and high diversity plots in 2003: DES (Wilcoxon rank sum test, W = 605, P = 0010), HSU (W = 505, P = 0004), HSP (W = 730, P = 0038), HEP (W = 400 P < 0001), CGC (W = 370, P < 0001), CWS (W = 700, P = 0028) and also in 2005: HSU (W = 330, P < 0001), HEP (W = 585, P = 0009, CPO (W = 680, P = 0024), see Appendix S3). The interaction webs showed three outstanding patterns (Fig. 3ad, Fig. 4): (i) both webs derived from the high plant diversity plots showed a consistently higher total connectance, interaction diversity and mean IS when compared with webs from the low plant diversity plots. (ii) The interaction webs from 2005 showed higher total connectance and total interaction diversity compared with the 2003 webs. (iii) Plantherbivore interactions as well as herbivorecarnivore interactions were consistently more frequent, more diverse and stronger in the high diversity plots, while the response of the other types of interactions was rather inconsistent. In general, the least observed interaction type was plant carnivore interaction (Fig. 4). Furthermore, IS was increased in the high diversity plots for all kinds of interactions in 2003. In 2005, this was only true for the vertical interactions, while the strength of horizontal interactions was decreased in the high diversity plots. These patterns were observed to be

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8 M. Rzanny & W. Voigt

(a) Low plant diversity; 2003 (c)
Low plant diversity; 2005

OMG

CPO

CGC

CWS

CVS

CGS

OMG

CPO

CGC

CWS

CVS

CGS

DES HSU HRF HSC HSP HEP

DSS

DES HSU HRF HSC HSP HEP

DSS

PSH

PGR

PTH

PLG

PSH

PGR

PTH

PLG

(d) High plant diversity; 2005 (b) High plant diversity; 2003
OMG CPO CGC CWS CVS CGS

OMG

CPO

CGC

CWS

CVS

CGS

DES HSU HRF HSC HSP HEP

DSS

DES HSU HRF HSC HSP HEP

DSS

PSH

PGR

PTH

PLG

PSH

PGR

PTH

PLG

Fig. 3. Interaction webs showing all signicant partial mantel correlations (links) between two functional groups. Black lines represent interactions assumed to trophic, while grey lines represent interaction assumed to be of non-trophic nature. Straight lines represent vertical interactions while upwardly curved lines represent horizontal interactions and downwardly curved lines represent interactions between herbivorous functional groups and detritivorous functional groups. Line width represents IS as indicated by the partial Mantel correlation (range of values: 016 < rM <063). See Table 2 for abbreviations of functional groups.

independent of the chosen alpha level (Fig. 4). Herbivore herbivore connectance and interaction diversity was higher in 2003 compared with 2005, but in both years constant for the two plant species richness levels (Fig. 4). However, this does not hold if alpha is increased to 01. Further exploration of the different interaction webs revealed differences in the linkages of their component functional groups (Fig. 3). Interactions between HSU and CPO were detected in each of the four interaction webs. Interestingly, in the 2003 interaction networks, CGS was isolated and CWS, both comprised of almost exclusively spiders, showed only one signicant horizontal interaction in each case but no interaction with any herbivore functional group. In contrast, both groups belong to the most strongly connected carnivore functional groups in 2005. Some functional groups were comparatively scarcely linked to other functional groups, for example, grasses (PGR), HSP and HSC, while others showed consistent, manifold interactions to other functional groups such as CPO, legumes (PLG), HSU and HRF. Especially in 2005, DSS shows many and strong associations with the carnivore functional groups.

Discussion
FUNCTIONAL GROUP ALLOCATION

There are various ways to classify arthropods to account for their ecological differences, ranging from taxonomic classications (Schaffers et al. 2008), guilds (Novotny et al. 2010) and subjective ad hoc classications (Perner & Voigt 2007) to much less applied rigorous and objective, statistical classications, most often restricted to selected taxa (e.g. hoveries: Schweiger et al. 2007). Whole ecosystem approaches, aiming to classify a major part of the entire community, are usually restricted to a priori subjectively dened feeding guilds (e.g.: Moretti, Duelli & Obrist 2006; Novotny et al. 2010). The allocation of species to such groupings usually requires many subjective decisions and is always subject to a serious degree of arbitrary assignments (Bengtsson 1998; Wilson 1999). To overcome these shortcomings, we adopted a datadriven approach applying more objective classication criteria. Although our approach still bears some kind of subjectiv-

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Plant diversity and multitrophic interactions 9

Total
06

P-H
(a) (d)

H-C
(g)

P-C
(i)

H-H
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Fig. 4. Network descriptors for the functional group interaction webs for low plant diversity mixtures (Low) vs. high plant diversity mixtures (High) using data from the years 2003 and 2005. Total values refer to network descriptors of the complete web (ac), and the remaining graphs refer to interactions between functional groups of two specic trophic levels (dk) or within the same trophic level (horizontal interactions, (lq)). P-H, Plantherbivore interaction; H-C, herbivorecarnivore interaction; P-C, plantcarnivore interaction; H-H, herbivoreherbivore interaction; C-C, carnivorecarnivore interaction.

ity (e.g. the decision of which traits to include in the calculation of the distance matrix), a great variety of incorporated relevant functional traits allows for a rigorous and more realistic functional differentiation among species. As expected, the functional groupings are principally driven by differences in feeding ecology. However, trophic grouping structure is complemented with other non-feeding related traits such as the vertical distribution (CVS vs. CGS), ignored by guild-specic approaches. For example, CGS and CVS show very different interaction patterns in all interaction webs (Fig. 3ad). The main advantages of our approach are the reproducibil-

ity, the unambiguous allocation of species with fuzzy traits and the simultaneous incorporation of multiple, potentially important classication criteria.

DIFFERENCES BETWEEN INTERACTION WEBS OF HIGH AND LOW PLANT DIVERSITY COMMUNITIES

We show that plant species richness affects interaction web complexity in terms of connectance, interaction diversity and IS. Highly connected communities are considered more robust to species loss (Dunne, Williams & Martinez 2002,

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology

10 M. Rzanny & W. Voigt 2004). Likewise, increased interaction diversity is likely to increase and stabilize the rate of ecosystem processes (Tylianakis et al. 2010). Increased IS refers to a stronger interdependence of the linked functional group members accompanied with higher robustness of this link. Consequently, we expect the entire community based on the more diverse plant communities to show increased insurance of ecosystem functioning and to be more robust to potential perturbations. Plant species richness effects cascade up the trophic chain and cause a marked increase in the interactions between adjacent tropic levels. Higher interaction web complexity following an increase in plant species richness is consistent in both sampling years (Fig. 4). Our results provide evidence for the existence of a mechanistic link between increased plant species richness and increased interaction diversity. Hence, our ndings support the view that interactions in grasslands can be strongly controlled by bottom-up forces (Price 2002; Boyer et al. 2003). This is in line with a previous analysis of functional group interaction webs in natural grasslands by Perner & Voigt (2007). They found a generally higher connectance of functional group interaction webs in a long-grown, highly diverse grassland located in an undisturbed nature reserve compared with a frequently disturbed and less diverse grassland situated nearby a fertilizer factory. Plant species richness was much lower in the disturbed grassland as a result of the exposure to strong emissions. This hence suggests that the changes in observed connectance of functional groups are at least partially mediated through higher species richness in the producer functional groups. Similar results were obtained by a study measuring interaction diversity in quantied insect food webs (Albrecht et al. 2007). The authors observed higher interaction diversity in restored meadows compared with intensively managed meadows. As an explanation, they suggested a mechanistic chain: restoration of agricultural land leads to increased plant species richness, which in turn increases insect species diversity and interaction diversity. Here we could experimentally corroborate this suggestion. A third study analysing functional group interaction webs in marine macrofaunal communities (Thrush, Coco & Hewitt 2008) concluded that lower diversity is likely to decouple functional group interactions and reduce ecosystem functionality. Although all the referred studies used data from different systems, different time-scales and analysed different species aggregation levels, they all draw a consistent conclusion, further conrmed by the present experimental study: Decreasing diversity reduces the complexity of interactions among community members. This is true for the total number of interactions. But a closer look at the different types of interactions reveals a much more differentiated response. Producerherbivore, herbivorecarnivore and to a certain degree carnivorecarnivore interactions represent for the most part trophic interactions, while herbivoreherbivore and producercarnivore interactions are dominated by non-trophic interactions. These latter types of interactions were generally rarer and showed rather inconsistent changes and idiosyncratic patterns with increasing plant species richness in the different sampling years (Fig. 4). For both plant species richness levels, the same plots share only one of fourteen links (low plant diversity plots, Fig. 3ac) or one of twelve links (high plant diversity plots, Fig. 3bd) of these non-trophic interactions in the two different years. This reects the extreme context dependency and temporal plasticity of non-trophic interactions, showing great variations in magnitude and sign across different communities (Berlow 1999). Furthermore, mean IS was increased in the high plant diversity plots in all interaction webs and all types of interactions with exception of the 2005 horizontal interactions. A possible reason for the observed higher connectance and IS in the more diverse plots is that more diverse producer communities are likely to support more diverse consumer communities (Siemann 1998; Scherber et al. 2010). Communities with greater taxonomic diversity are also likely to be more structurally heterogeneous and thus provide a greater variety of complemental resources, which in turn support a greater variety of interactions (Denno, Finke & Langellotto 2005). There are signicant differences in species richness between some functional groups across the two plant species richness levels (Appendix S3), so this might be one reason for the observed higher interaction web complexity. However, if such a relationship would be generally present, it would become apparent in the form of a positive relationship between the signicant partial Mantel correlations and the summarized mean species richness of the interacting functional groups. Alternatively, the fraction of realized links per functional group may be related to their mean species richness. However, there is neither a signicant relationship between mean rM and species richness within functional groups (pooled for 2003 and 2005 and both plant species richness levels (F1,112 = 218, P = 0143, Appendix S4)) nor a signicant relationship between the mean number of species per functional group and the fraction of realized links (F1,65 = 340, P = 0070, Appendix S5), suggesting that the number of species within a certain functional group per se is neither indicative of their IS with other functional groups nor is it indicative of the number of links connecting this functional group. Accordingly, our results are not biased by an increased number of species per functional group. This leads to the conclusion that interaction structure is altered independently of the species richness of the interacting functional group. This is in accordance with another species-based food web study (Tylianakis, Tscharntke & Lewis 2007) that showed that habitat modication altered the structure of hostparasitoid food webs without changing species richness. This underlines the importance of using species interactions as a response variable in further studies to adequately capture and monitor changes in community structure and function. More simple structured systems still feature their basic functionality, but they rather lack their robustness and tolerance to disturbance (Dunne, Williams & Martinez 2002; Parrott 2010).

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology

Plant diversity and multitrophic interactions 11 species interactions argues for a whole system approach (Ives & Cardinale 2004) to compare the structural properties and differences of the resulting interaction networks independent of the specic species composition.

DIFFERENCES BETWEEN THE SAMPLING YEARS

The interaction webs for 2003 generally showed lower values for most complexity descriptors when compared with the 2005 interaction webs. These obviously simpler interaction structures become additionally evident in the number of isolated or sparsely linked functional groups in 2003 for both diversity levels (CGS, CWS). The main reason for this is probably a limited time span for the establishment of species interactions in the 2003 sampling period. The plant communities were one and a half years old when the arthropods in 2003 were sampled. Ecological networks are known to show high temporal plasticity (Olesen et al. 2008; Petanidou et al. 2008) and at the beginning of the experiment in 2003, a high species turnover occurred through the establishment of the experimental grasslands on former arable elds (Roscher et al. 2004). Stable interactions among functional groups did not develop during the rst year of community establishment, as the process of self-organization and maturation of ecological networks requires more time (Mu ller 2005; Parrott 2010). In the case of plantcarnivore interactions, the response to changing plant species richness is the converse in both years. However, there are only a few links of this type present, which occur between different pairs of functional groups, suggesting more or less transient, loosely and unpredictable interactions. Principally, the same is true for the herbivoreherbivore interactions. These interactions are more frequent in 2003 compared with 2005, while connectance is constant for both plant species richness levels. Furthermore, IS is increasing with plant species richness in 2003 but decreasing in 2005. These apparently idiosyncratic patterns, which are probably superimposed by species-specic invasion patterns, suggest transient and species-dependent forces determining horizontal interactions, which encompass species-specic direct and indirect competition or even facilitation effects, that is, the members of a functional group will hardly behave equally in these highly heterogeneous interaction types.

FUNCTIONAL GROUP- VS. SPECIES-BASED APPROACHES

SPECIFIC FUNCTIONAL GROUP INTERACTION PATTERNS

The establishment and analysis of quantitative species-based interaction webs have greatly improved our understanding of a variety of mechanisms (Bascompte & Jordano 2007; Ings bault & Fontaine 2010). This popular eld of et al. 2009; The ecological network analysis stimulates both theoretical and empirical research including conservation biology (Tylianakis et al. 2010). However, creating species-based interaction webs of at least approximately complete multitrophic arthropod communities requires the simultaneous measuring of different types of interactions among hundreds if not thousands of species, which are often very difcult to detect and much less to quantify. However, the more complex a system is, the more accurate must be the quantication of IS to enable the prediction of community dynamics (Novak et al. 2011). In contrast to species-based interaction webs, functional group-based interaction webs permit an efcient view on whole community organization without the need to observe different types of species interactions directly. Instead, interactions are inferred from abundance matrices thereby covering all different kinds of interactions leading to changes in species abundance. Unlike species-specic measured interactions, these links represent undirected interactions and cannot distinguish mutualistic and antagonistic interactions (i.e. they consider the degree of dependence of functional groups). Because of the idiosyncrasy and context dependency of specic species interactions, a functional group approach reveals structural differences of interaction webs on an appropriate scale enabling the comparison of communities comprised of completely different species. Representing communities as functional group interaction webs provides an important step towards a more general view of ecosystems, enabling comparisons between different ecosystems on a global scale.

In some cases, strong interactions exist between functional groups in low plant diversity plots, which are not present in more diverse plots, for example, HSU-CVS. The presence and strength of a link between two functional groups is dependent on the specic species composition of this group, which is strongly varying over the replicate plots because of the (restricted) random allocation of plant species to the community mixtures. Mutual interactions among individuals of different functional groups are dependent on the context of the interplay of abiotic and biotic environments. Additionally, population size and specic interaction frequencies are known to vary from year to year even in the same ecosystem (e.g. Schmidt & Tscharntke 2005; Petanidou et al. 2008). Hence, specic interaction web patterns will equally vary across the plots and years. This idiosyncrasy of specic

Conclusions
Our results revealed that the loss of plant biodiversity has important implications for functional group interactions across three trophic levels. This underlines the fact that plant diversity is of vital importance for community structure and functioning. The observed greater interaction diversity and connectance in communities based on diverse plant communities have the potential to increase and stabilize the rate of diverse ecosystem processes (Tylianakis et al. 2010), thereby probably enhancing network stability. Structural measures of interaction networks, such as ecosystem complexity, have the potential to act as a key ecological indicator, providing means to monitor their functional state and assess, for instance, the success of conservation or restoration efforts.

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology

12 M. Rzanny & W. Voigt However, there is still a great need to establish a commonly agreed standard procedure including a common core list of traits for classifying arthropod functional groups.
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Acknowledgements
The Jena Experiment has been funded by the Deutsche Forschungsgemeinschaft (DFG, Wi 1601 4-1,-2, FOR 456), with additional support from the Friedrich Schiller University of Jena and the Max Planck Society, and the trait data base to classify functional groups has been engendered as part of another DFG project (VO 795 3-1). We thank all the colleagues and people who maintained the Jena Experiment and those who provided basic plant data (e.g. biomass), in particular Vicky Temperton, Christiane Roscher and Alexandra Weigelt, as well as numerous student helpers who sorted arthropods out from litter. Markus Lange, Esther Kowalski and Dirk Lauterbach (2003), and Ramona Mu ller and Annely Kuu (2005) kindly contributed data for some arthropod taxa. Tina Buchmann, Andreas Lindig and Kristin Schu fer helped to develop the trait data base. We are also very grateful to Hugh Loxdale, Mary F. Voigt, Jan Engel and three reviewers (Oliver Schweiger and two anonymous reviewers) for helpful comments. MR acknowledges funding by the German Federal Foundation for Environment (DBU).

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Supporting Information
Additional Supporting Information may be found in the online version of this article. Table S1. List of all arthropod species included in the analysis and their classication into functional groups. Appendix S1. Contribution of each variable to the global distance (calculated following Pavoine et al. 2009).

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology

14 M. Rzanny & W. Voigt

Appendix S2. Average silhouette width plotted against the cutting level (number of clusters) of the cluster diagram. Appendix S3. Species richness of the arthropod functional groups in 4plant species mixtures (SD4) compared to 16plant species mixtures (SD16) for (a) 2005 and (b) 2003. Appendix S4. Scatter plot showing no relationship between signicant partial Mantel correlation coefcients (rM) and the summarized species richness of the functional groups (FGs; Adj. r2 = 0010; P = 0143). Appendix S5. Scatter plot showing no signicant relationship between the fraction of realised links and the mean species richness per functional group. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be reorganised for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing les) should be addressed to the authors.

2012 The Authors. Journal of Animal Ecology 2012 British Ecological Society, Journal of Animal Ecology