Land‐Use Effects on the Functional Distinctness of Arthropod Communities

Ecography 38: 889–900, 2015 doi: 10.1111/ecog.01141 © 2015 Th e Authors. Ecography © 2015 Nordic Society Oikos Subject Editor: Catherine Graham. Editor-in-Chief: Miguel Ara ú jo. Accepted 18 November 2014

Land-use effects on the functional distinctness of arthropod communities

Klaus Birkhofer , Henrik G. Smith , Wolfgang W. Weisser , Volkmar Wolters and Martin M. Gossner

K. Birkhofer ([email protected]) and H. G. Smith, Dept of Biology, Lund Univ., S ö lvegatan 37, SE-223 62 Lund, Sweden, and Centre of Environmental and Climate Research, Lund Univ., SE-223 62 Lund, Sweden. – W. W. Weisser and M. M. Gossner, Terrestrial Ecology Research Group, Dept of Ecology and Ecosystem Management, Center for Food and Life Sciences Weihenstephan, Technische Univ. Mü nchen, Hans- Carl-von-Carlowitz-Platz 2, DE-85354 Freising, Germany. – V. Wolters, Dept of Animal Ecology, Justus Liebig Univ., Heinrich-Buﬀ -Ring 26-32, DE-35392 Giessen, Germany.

Land-use change is a major driver of the global loss of biodiversity, but it is unclear to what extent this also results in a loss of ecological traits. Th erefore, a better understanding of how land-use change aff ects ecological traits is crucial for eff orts to sustain functional diversity. To this end we tested whether higher species richness or taxonomic distinctness generally leads to increased functional distinctness and whether intensive land use leads to functionally more narrow arthropod communities. We compiled species composition and trait data for 350 species of terrestrial arthropods (Araneae, Carabidae and Heteroptera) in diff erent land-use types (forests, grasslands and arable fi elds) of low and high land-use intensity. We calculated the average functional and taxonomic distinctness and the rarifi ed trait richness for each community. Th ese measures refl ect the range of traits, taxonomic relatedness and number of traits that are observed in local communities. Average functional distinctness only increased signifi cantly with species richness in Carabidae communities. Functional distinctness increased signifi cantly with taxonomic distinctness in communities of all analyzed taxa suggesting a high functional redundancy of taxonomically closely related species. Araneae and Heteroptera communities had the expected lower functional distinctness at sites with higher land-use intensity. More frequently disturbed land-use types such as managed grasslands or arable fi elds were characterized by species with smaller body sizes and higher dispersal abilities and communities with lower functional distinctness or trait richness. Simple recommendations about the conservation of functional distinctness of arthropod communities in the face of future land-use intensifi cation and species loss are not possible. Our study shows that these relationships depend on the studied taxa and land-use type. However, for some arthropod groups functional distinctness is threatened by intensifi cation and conversion from less to more frequently disturbed land-uses.

Land-use change, here defi ned as anthropogenic changes negative eff ects of land-use change on species richness made to the biophysical attributes of the earth ’ s surface is expected if the functional diversity of communities is (Lambin et al. 2001), includes two components (Foley et al. positively related to species richness. If so, conservation 2005): the conversion of one land-use type into another eff orts that target species richness would incidentally con- (e.g. forest to arable land), and the degree of anthropogenic serve functional diversity ( ‘ sampling eff ect hypothesis ’ , disturbances (e.g. increasing timber harvesting or fertiliza- Mayfi eld et al. 2010). In contrast, the concept of functional tion). Land-use change has been identifi ed as a major driver redundancy suggests that species may be mutually substi- of the global loss of biodiversity (Sala et al. 2000) and can tutable regarding ecosystem functionality (Bl ü thgen and be accompanied by a loss of functional traits from commu- Klein 2011). Consequently, it has been argued that a loss nities that may aff ect ecosystem functioning (Duff y 2009). of species may not simultaneously cause a loss of functional Th e conservation of species richness by mitigating negative traits because of such functional redundancy (Hillebrand eff ects of land-use conversion or intensifi cation may there- and Matthiesen 2009, Cadotte et al. 2011, Gravel et al. fore result in improved ecosystem functionality (Cardinale 2012, Mouillot et al. 2013). et al. 2012). Functional complementarity between species in local Th e concept of functional complementarity suggests that communities has been documented over a range of plant two species in a community together contribute more to and animal taxa, primarily by relating measures of func- ecosystem functionality than each one alone (Loreau and tional diversity to productivity or biomass estimates (Loreau Hector 2001), whereas two species are functionally redun- et al. 2001, Balvanera et al. 2006, Cardinale et al. 2006, dant if they contribute equally to ecosystem functionality Hooper et al. 2012). However, the ongoing debate on the (Rosenfeld 2002). A loss of functional diversity due to relative importance of functional complementarity versus

889 redundancy is refl ected by a number of studies that focus communities refl ects the functional distinctness of commu- on the relationship between species richness and functional nities better than species richness and may be a valid proxy diversity in plants and vertebrates (Flynn et al. 2009, Villé ger for functional distinctness in cases where trait information is et al. 2010, Baraloto et al. 2012, Lavorel 2013). Cadotte not available for all species (see also D í az et al. 2013). et al. (2011) reviewed the evidence for the generality of this We compiled trait data for 350 species in communi- relationship in plant communities and concluded that func- ties of three abundant terrestrial arthropods taxa (Araneae, tional diversity can change with minimal changes in species Carabidae and Heteroptera) to analyze how species diver- richness. Mayfi eld et al. (2010) came to the same conclusion, sity, average taxonomic and functional distinctness of com- but emphasized that species richness and functional diversity munities are aff ected by: land-use type (forest, grassland may not always be related and that these relationships may and arable land) and intensity (low and high; Table 1). depend on the land-use context (see also Petchey and Gaston Th e selected terrestrial arthropod groups are abundant 2006). Our understanding of the functional complementar- and provide important ecosystem services (e.g. Araneae, ity between invertebrate species is less well developed than Carabidae and Heteroptera as biological control agents, for plants, and some studies suggest limited complemen- Symondson et al. 2002) or disservices (e.g. Carabidae and tarity between functional groups. For example, functional Heteroptera as pests, Alford 2011). All groups, however, groups of Araneae species (web-builders and cursorial spe- diff er greatly in their morphological and ecological traits, e.g. cies, Birkhofer et al. 2008) or major functional groups of Araneae are unable to fl y but partly show ballooning behav- arthropod predators (generalists and specialists, Diehl et al. ior during dispersal; Carabidae are mostly ground-dwelling, 2013) do not show complementarity with regard to pest but partly fl ight-capable; most Heteroptera are fl ight-active. control in crops. It further remains unknown if eff ects of Th us responses to land use are expected to diff er between environmental change on functional diversity (e.g. climate major taxonomic groups. Understanding how diff erent change, Ruhí et al. 2013) are independent of species richness aspects of their diversity respond to land-use change will (Hooper et al. 2005). Hence, determining if species richness therefore contribute to improve future conservation eff orts and functional diversity are positively related and respond that may target the conservation of functional diversity in in similar ways to land-use change will help to improve addition to species richness. We further related species rich- eff orts that target the conservation of functional diversity in ness, taxonomic distinctness and functional distinctness of terrestrial arthropod communities. arthropod groups with diff erent feeding preferences to each Studies that focus on the functional diversity of other in a context dependent manner (per taxon, land-use terrestrial arthropod communities and their relationship to type and intensity) to understand if general recommendations species richness have been hampered by the large number of could lead to the conservation of several aspects of diversity species that usually characterize arthropod communities and simultaneously and independent of context (Mayfi eld et al. the limited knowledge about traits for all species (but see for 2010). We address the following questions: 1) does higher example Moretti et al. 2009, Bihn et al. 2010, Vandewalle species richness generally result in higher functional distinct- et al. 2010). To overcome this problem, it has been ness of communities? (complementarity of species), 2) does suggested that phylogenetic diversity may be a valid indica- higher taxonomic distinctness lead to increasing functional tor of functional diversity (Huang et al. 2012) and may even distinctness of communities and is this eff ect independent of be a proxy for ecosystem functioning (Srivastava et al. 2012). changes in species richness or land-use diff erences? (comple- Th is assumption holds for communities in which distantly mentarity of unrelated species) and 3) do higher land-use related species share fewer traits compared to closely related intensities or more frequently disturbed land-use types such species (Bracken and Low 2012, Dí az et al. 2013), i.e. when as agricultural land lead to arthropod communities in which traits are phylogenetically conserved. To address aspects of species are functionally more similar or have a lower trait relatedness between arthropod species in local communities richness? (functionality). Finally, to emphasize the applied in absence of complete phylogenies for our study taxa we aspects of our study for conservation planning, we also pro- calculated the average functional and taxonomic distinct- vide information about traits that are particularly threatened ness of each community. Th e functional distinctness is the if land use is intensifi ed or if land-use types would be con- average resemblance between all pairs of species in a given verted. community based on the observed traits and describes the average functional breadth of communities (Somerfi eld et al. 2008). It is complementary to a measure of functional Methods diversity (FD) that is based on hierarchical clustering and describes the functional diversity of a community as the total Study regions and datasets branch length in a dendrogram (Petchey and Gaston 2002). Th e taxonomic distinctness is based on the relatedness We compiled data collected in individual studies that between species in Linnaean classifi cation trees (Clarke and were conducted in three study regions in central Germany Warwick 1998) and is mathematically related to the average (Fig. 1). We combined individual datasets to derive data from functional distinctness. It has recently been suggested as an three dominant land-use types in Germany and from six sites indicator of phylogenetic diversity if phylogenetic informa- of low and high management intensity each per land-use tion is not available and covers important aspects of func- type (Table 1; for more details on sampling and study region tional diff erentiation between species (Griffi n et al. 2013) see Supplementary material Appendix 1). Th ree groups and responses to land-use change (Andersson et al. 2013). of terrestrial arthropods (Araneae, Coleoptera: Carabidae We assume that the average taxonomic distinctness of and Hemiptera: Heteroptera) were selected, because 1) they

890 Table 1. Overview of site characteristics, land use and sampling properties per region for Araneae, Carabidae and Heteroptera at forest, managed grassland and arable sites. Additional information is provided in Supplementary material Appendix 1.

Land-use type Forest Grassland Arable land Region Hainich-Duen (Thuringia) Wetterau (Hesse) Northeim (Lower Saxony) Coordinates 10.77917 ° – 10.17332 ° E, 51.37872 ° – 50.93735 ° N 8.768463 ° E, 50.232493° N 9.995906 ° E, 51.700179 ° N Annual mean 6.5 – 8.0 9.1 – 10.0 8.7 temperature [° C] Annual precipitation 500 – 800 500 – 700 645 [mm] Land-use intensity Unmanaged beech vs Low (LUI 0.55 – 0.64) Organic vs conventional Organic cereal fi elds vs managed age class beech vs high (LUI cereal fi elds (Araneae, grassy fi eld margins (age 80) 2.18 – 2.74) Carabidae) (Heteroptera) land-use intensity* Sampling method Pit-fall traps, fl ight- Pit-fall traps, Pit-fall traps Suction sampling interception traps sweep-netting Sampling period April – October 2008 April– October 2008 May – June 2007 June – July 2008 * LUI-index summarizes the standardized intensity of three components of land use; fertilization, mowing, and livestock grazing (Bl ü thgen et al. 2012). represent a range of trophic levels (Araneae, strictly carnivo- Trait characterization rous; Carabidae, carnivorous and herbivorous, seed eating as well as omnivorous species; Heteroptera, carnivorous We defi ne a trait as a morphological, phenological or eco- and herbivorous, plant-sap sucking as well as omnivorous logical feature of a species that may aff ect its performance species), 2) they diff er in their morphological and ecologi- or fi tness (Table 2). Our selection of traits was constrained cal traits and thus might respond diff erently to land use, 3) to those traits that were available for all 350 species in they are numerically and functionally important in terres- the analyzed communities (for a species traits list see trial ecosystems, and 4) information on traits and taxonomic Supplementary material Appendix 2). Th e three analyzed classifi cation was available for all 350 species. Our results arthropod groups contribute to a range of diff erent func- are based on a comprehensive dataset for Araneae (143 spe- tions and instead of focusing on a single function or ser- cies, 10 498 individuals), Carabidae (116 species, 19 903 vice (and a subset of corresponding traits) we assembled a individuals) and Heteroptera (91 species, 2877 individuals) range of traits that characterize the species’ location in trait communities in forests, grasslands and arable fi elds of con- space within each community. We collected information for trasting land-use intensities. each Araneae, Carabidae and Heteroptera species that refl ect categories of morphological (body size range), phenological (reproductive biology) and ecological (feeding biology, dispersal ability and stratum utilization) traits (Table 2 and Supplementary material Appendix 3). We converted trait categories to a series of binary coded variables, as such an approach has the advantage that a species does not have to be assigned a specifi c value (e.g. mean body size), but could instead fall into a range of for example body-size categories. Th e number of variables which constitute such coding of a trait category implies a weighting for that trait category and we therefore constrained the number of trait variables in each category to 2 – 4 (Table 2, see also Somerfi eld et al. 2008).

Community analyses

We calculated the following measures for all communities: a) species richness, b) average taxonomic distinctness ( Δ ), c) average functional distinctness ( X ), d) residuals of average functional distinctness ﬁ tted for average taxonomic distinctness ( X ∼ Δ ), e) rariﬁ ed trait richness and f) relative trait composition of arthropod communities at each site. Measures b – f are not commonly applied in biodiversity studies and are explained in more detail. Th e average taxonomic distinctness (Δ ) was calculated based on two matrices: 1) a sites species matrix with Figure 1. Map of the three study regions in Germany, point presence/absence records for all species and 2) a matrix location are approximate centers of each study area. that provides information about the taxonomic relatedness

891 Table 2. Overview of trait categories and trait selection for binary coding in Araneae, Carabidae and Heteroptera. Note that several traits within a category could be coded with 1, for example if a Carabidae species is known to be herbivorous and carnivorous. The number of classes in each category is given in square brackets; species traits lists are provided in Supplementary material Appendix 2, references for the traits are given in Supplementary material Appendix 3.

Trait category Araneae Carabidae Heteroptera Morphology Body length Coded as cont. 5 mm classes, Coded as cont. 5 mm classes, Coded as cont. 5 mm classes, ranging from 0 – 5 mm to 10 ranging from 2 – 7 mm to ranging from 0 – 5 mm to mm [3] 17 mm [4] 10 mm [3] Phenology Reproductive Coded as season with adult Coded as season with adult Coded as season with adult biology individuals, winter, spring, individuals, spring and autumn individuals, winter, spring, summer and autumn [4] breeders [2] summer and autumn [4] Ecology Feeding Hunting mode coded as cursorial, Trophic level coded as Trophic level for adults coded biology sheet-web and aerial carnivorous and as carnivorous, herbivorous web-builder [3] herbivorous [2] or mycetophagous [3] Dispersal Ballooning and migration Wing morphology coded as Wing morphology coded as ability propensity coded as low- brachypterous and brachypterous and intermediate and good-high [2] macropterous [2] macropterous [2] Stratum Stratum preference coded as Stratum preference coded as Stratum preference coded as utilization surface and vegetation [2] surface and vegetation [2] surface, herb and shrub/tree vegetation [3]

between species. We derived information on taxonomic Th is distance measure not only characterizes the resemblance categories and classifi cation of species from the Fauna between two species for shared traits (presence of the same Europaea database (Araneae: species, genus and fam- trait in two species), but also considers the absence of a trait ily; Carabidae: species, genus, tribe and subfamily and in two species to calculate resemblance. Th e rationale behind Heteroptera: species, genus, family, superfamily and this approach is that both overlap in traits (e.g. both species infraorder; Fauna Europaea, ‘ Taxonomic Hierarchy ver. are carnivorous), as well as the absence of certain traits in [2.5]’ (2012); for classifi cation trees see Supplementary two species (e.g. both species do not have adults in winter), material Appendix 4) and used the additional category describe the functional distinctness between species in cases Entelegynae for spiders (the monophyly of the latter is where trait information is available for all species and traits supported by molecular analyses, Agnarrson et al. 2013). (our data fulfi ls this criterion). We acknowledge the range of Based on this information of taxonomic relatedness between available measures to calculate diff erent aspects of functional species, we defi ned the step length for the highest level diversity (Mouchet et al. 2010), but chose the average func- of un-relatedness between two species in a community as tional distinctness measure as it defi nes the extent of trait 100 (e.g. two Heteroptera species from diff erent infraorders). diff erences between species in a local community (D í az and Depending on the number of taxonomic levels in each of Cabido 2001), allows for a coding in accordance with the the three analyzed arthropod groups, species show diff erent available traits for all analyzed species, and is related to the levels of relatedness (e.g. 100 for a Cimicomorpha versus measure of average taxonomic distinctness. As data comes a Pentatomorpha species; 80 for two species that are both from diff erent studies taxonomic and functional distinctness Cimicomorpha, but are from diff erent superfamilies; 60 for measures were further selected because they are independent two species that are from the same superfamily, but diff erent of sample size and solely based on average pairwise distances families, 40 for two species from the same family, but dif- between all possible species pairs in a community (Clarke ferent genera and 20 for two species from diff erent species and Warwick 1998). Th e measure X ∼ Δ is given by the but the same genus). Based on these values for taxonomic residuals of a simple linear regression between average taxo- distinctness between pairwise comparisons of species, the nomic distinctness ( Δ ) and average functional distinctness average taxonomic distinctness between all species pairs in ( X ) in each of the three analyzed arthropod groups. Th is a community can be calculated. Th e average taxonomic dis- dependent variable describes the functional distinctness of a tinctness has previously been documented as an important community while accounting for the taxonomic relatedness diversity measure in addition to species richness (Paschetta between species and is therefore independent of taxonomic et al. 2012, Birkhofer et al. 2014b) and is recommended for relationships. studies with communities from spatially separated regions Th e rarifi ed trait richness (TR) was calculated based on a (Schweiger et al. 2008). site trait matrix with the number of species that possess a Th e average functional distinctness (X , Somerfi eld et al. certain trait variable given for each site. From this table we 2008) resembles the average taxonomic distinctness, but is identifi ed the site with the lowest number of total species based on a fi le that describes trait values for all species instead coding for all traits. Th is species number was then used to of taxonomic information to defi ne resemblance between rarify trait richness at all sites to the level of the site with the species. Using resemblances between species, the average lowest number of species. Th e resulting rarefi ed trait richness functional distinctness ( X ) between species in a community is the expected trait richness at each site assuming all sites can be calculated based on the information which species would have exactly the same minimum number of species. are present in a community. We followed the approach by To analyze trait composition (TC) we used the same site x Somerfi eld et al. (2008) and used the simple matching coeffi - trait matrix that was used for TR estimates. To account for cient to characterize trait-based resemblances between species. diff erence in the number of species between trait variables

892 we then standardized species counts in each trait variable by Table 3. Pearson correlation coefﬁ cients for the relationship the maximum species number. A value of 100 for a single between species richness (S), average taxonomic distinctness (Δ ) and average functional distinctness (X ) of Araneae, Carabidae and trait variable suggests that at this particular site, the high- Heteroptera communities (N 36 for Araneae and Carabidae; N 34 est number of species was observed that showed this trait for Heteroptera, excluding two sites with only a single species). across all sites. Th ese percentage values for all trait variables provide a matrix of sites traits that indicate the dominance S Δ of trait variables in terms of the standardized number of spe- Araneae cies showing that trait at each site. Th is multivariate table on Δ R 0.31; p 0.064 1.00 trait composition (TC) data was further analyzed to detect X R 0.31; p 0.070 R 0.46; p 0.005 Carabidae which traits were dominant in particular land-use intensi- Δ R 0.39; p 0.019 1.00 ties or types. Ultimately, these dominances of traits suggest X R 0.45; p 0.007 R 0.45; p 0.006 if particular traits that are represented by species would be Heteroptera threatened by land-use intensiﬁ cation or conversion. Δ R 0.19; p 0.291 1.00 X R 0.25; p 0.156 R 0.61; p 0.001

Statistical analyses taxa (Table 3). Th is relationship remained signifi cant after For statistical tests all univariate measures were used to accounting for species richness (N 36, Araneae: Rpartial calculate individual resemblance matrices between sites 0.40, p 0.016; Carabidae: R partial 0.34, p 0.047; based on Euclidean distances. Th e multivariate table on trait N 34, Heteroptera: Rpartial 0.59, p 0.001). composition was transformed into a resemblance matrix If analyzed for diff erent land-use intensities, Carabidae using Bray– Curtis distances. Each resemblance matrix was and Heteroptera average functional distinctness and taxo- individually tested for each analyzed arthropod group against nomic distinctness were signifi cantly related in high (N 18, the null-hypothesis that the fi xed factors land-use type Carabidae: R 0.56, p 0.015; N 16, Heteroptera: (forest, grassland or arable) and intensity (low or high) and R 0.77, p 0.001), but not in low intensity plots their interaction as model terms, did not aff ect resemblance. (Fig. 2c, e). Th is relationship in high intensity plots Th e two-factorial, balanced design was analyzed by permu- tended to be signifi cant after accounting for species rich- tational analysis of variance (PERMANOVA) based on the ness in Carabidae communities (Rpartial 0.47, p 0.055) permutation of residuals under a reduced null model. 9999 and was signifi cant after accounting for species richness permutations were used to test for statistical signifi cance of in Heteroptera communities (Rpartial 0.73, p 0.002). main eff ects and the two-way interaction (Anderson 2001). Taxonomic and functional distinctness were signifi cantly Relationships between the average functional and taxonomic related in Araneae communities (Fig. 2a; N 36, R 0.46, distinctness were analyzed with Pearson correlations and par- p 0.005), a relationship that was not signifi cant for indi- tial correlations to control for species richness for each individual intensity levels. vidual land-use context (per land-use intensity and type). Regarding land-use types, average functional distinct- Correlations are shown depending on context if at least one ness and taxonomic distinctness of Araneae communities correlation within the land-use intensity or land-use type were signifi cantly related in arable fi elds and forests (N 12; context was signifi cant, otherwise overall correlations are arable: R 0.58, p 0.047; forest: R 0.67, p 0.016), shown independent of land-use intensity or type. All univar- but not in grasslands (Fig. 2b). Th is relationship tended to iate results are shown as median with 25 and 75 percentiles, be signifi cant after accounting for species richness in arable multivariate results on trait composition (TC) are shown as fi elds (Rpartial 0.59, p 0.058) and remained signifi cant in non-metric multidimensional scaling ordinations (NMDS). forests after accounting for species richness (Rpartial 0.83, Vectors for individual traits are superimposed in NMDS p 0.002). Th e average functional distinctness and taxo- plots for trait variables with a multiple correlation coeffi - nomic distinctness of Carabidae communities were signifi - cient 0.3 to illustrate relationships between traits and lev- cantly related (Fig. 2d), a relationship that was not signifi cant els of land-use intensity or type. All statistical analyses were if tested for individual land-use types. Th e average functional performed using the software Primer-E ver. 6 (Clarke and distinctness and taxonomic distinctness of Heteroptera com- Gorley 2006) and the PERMANOVA add-on (Anderson munities were signifi cantly related in grasslands and forests et al. 2008). (N 12; grassland: R 0.79, p 0.002; forest: R 0.59, p 0.042), but not in arable fi elds (Fig. 2f). Th ese relationships in Heteroptera communities were not signifi cant after Results accounting for species richness.

Complementarity Functionality Species richness was signifi cantly and positively related to the average functional distinctness and average taxonomic Land-use intensity aff ected the average functional distinct- distinctness in Carabidae, but these relationships were ness in Araneae and Heteroptera communities depending on not signifi cant in Araneae and Heteroptera communi- land-use type (Table 4, X ) and this eff ect was independent ties (Table 3). Average taxonomic and functional distinct- of taxonomic distinctness (Table 4, X ∼ Δ ). Araneae com- ness were signifi cantly related to each other in all analyzed munities had a higher average functional distinctness in less

893 Figure 2. Relationship between average taxonomic distinctness ( Δ ) and average functional distinctness ( X ) for (a) and (b) Araneae, (c) and (d) Carabidae (N 36) and (e) and (f) Heteroptera (N 34) communities at low (᭡ ) and high (᭡ ) intensity sites and in forests (᭺ ), grasslands (᭹ ) and arable ﬁ elds (᭹ ). Note that N 34 in Heteroptera due to the presence of only a single species at two sites and that context dependent relationships are only shown for signiﬁ cant partial correlations at individual intensity levels or land-use types.

intensively managed forests and grasslands (Fig. 3a), but this nities had the highest functional distinctness in forest (Fig. eff ect was not present in forests after accounting for the taxo- 3e), but this diff erence was not present after accounting for nomic distinctness between species (Fig. 3b). In less inten- taxonomic distinctness (Fig. 3f). sively managed arable fi elds Araneae communities had a Th e rarifi ed trait richness in each community was signifi - lower average functional distinctness after accounting for the cantly aff ected by land-use type in Araneae and Heteroptera taxonomic distinctness of communities (Fig. 3b). Th e aver- communities (Table 4, TR), with richness being lowest in ara- age functional distinctness of Carabidae communities did ble fi eld for Araneae (Fig. 4a) and grasslands for Heteroptera not diff er signifi cantly between high and low intensity plots (Fig. 4c). Trait richness was higher in high intensity forest (Table 4). Th e average functional distinctness of Heteroptera and arable sites for Heteroptera (Fig. 4c) and at arable sites communities diff ered signifi cantly (Table 4), with a lower for Araneae (Fig. 4a). No signifi cant eff ects of land use on average functional distinctness in intensively compared to trait richness were observed in Carabidae. Th e composition less intensively managed grasslands and arable fi elds and a of traits in Araneae and Heteroptera communities diff ered higher average functional distinctness in high intensity for- signifi cantly between the three land-use types but depend- est plots (Fig. 3e). Th ese diff erences were also present after ing on land-use intensity, whereas the composition of traits accounting for taxonomic distinctness (Fig. 3f). in Carabidae communities only depended on land-use type Regarding land-use types, Araneae communities had (Table 4, TC). Species with a low to intermediate dispersal the highest functional distinctness in forests and the lowest range, that construct sheet-webs or large species ( 10 mm) functional distinctness in arable fi elds, with grasslands in- were characteristic for Araneae communities in forests (top between (Fig. 3a). Carabidae communities had the highest vs bottom part in Fig. 5a). Araneae communities in grass- average functional distinctness in grasslands (Fig. 3c), but lands were characterized by cursorial species that utilize the the magnitude of this diff erence was reduced by accounting soil surface and vegetation stratum and by species that have for taxonomic distinctness (Fig. 3d). Heteroptera commu- adults in summer or are good dispersers. Th e same group of

894

traits was also more characteristic for Araneae communities 0.004 0.018 0.001 0.001 0.001 0.001 at high compared to low intensity forest sites (right vs left

part in Fig. 5b). Th e presence of brachypterous, carnivorous and large ( 12 mm) Carabidae species was characteristic for

eld) and land- forest and grassland sites compared to communities at arable 3.6 9.1 2.9 14.7 39.6 26.4 sites (top vs bottom part in Fig. 5b). Carabidae communi- rable ﬁ rable

a ties in grasslands and arable ﬁ elds were further characterized by a more frequent presence of macropterous, phytophagous 0.030 0.021 0.013 0.001 or vegetation-dwelling species and species in the size ranges

from 2– 12 mm compared to forest communities (left vs right TR TC rassland or rassland

g part in Fig. 5b). Heteroptera species that have carnivorous or 3.9 4.6 6.9 mycetophagous adults or with preferences for the shrub/tree 72.9 orest, f stratum were characteristic for forest communities (top vs

1.8 0.182 1.7 0.196 bottom part in Fig. 5c). Low intensity plots in forests and grasslands were further characterized by Heteroptera species

and TR can be seen in Fig. 3, 4. Trait composition Trait 3, 4. TR can be seen in Fig. and

0.023 0.006 0.003 0.001

that were brachypterous (left vs right part in Fig. 5c). X

+ X

FpFpFp 4.3 6.2 0.3 0.7752.8 0.109 6.2 X 66.2 Discussion for

0.8 0.380 0.00 0.989 0.9Our 0.438 study revealed four main ﬁ ndings related to our initially addressed questions: 1) only Carabidae communities showed 0.032 0.001 0.001 0.001 0.001 0.001 0.010

a signiﬁ cant increase of average functional distinctness with

xed factors land-use type (levels: xed factors land-use type (levels: X

), average functional distinctness corrected for average taxonomic distinctness functional distinctness corrected for average ), average species richness; 2) the average functional distinctness

in Heteroptera are only 28 due to the presence of only a single species at two are only 28 due to the presence of a single species at two in Heteroptera

X increased signiﬁ cantly with average taxonomic distinctness 9.4 4.0 9.5 9.1 7.8 7.3 94.6

or independent of species richness in all analyzed arthropod taxa; 3) higher land-use intensity was not uniformly associ- f

a ated with a lower functional distinctness or trait diversity of h arthropod communities across the analyzed arthropod taxa g g l or the three diﬀ erent land-use types; 4) traits that characterize body size, dispersal abilities, foraging ecology and stra- a a f tum utilization where more indicative of particular land-use types than traits that characterized the reproductive biology 0.001 0.001 0.020

of species. Land-use type generally had a stronger eﬀ ect on Δ

), average functional distinctness ( ), average trait composition than land-use intensity, suggesting that the

composition of traits is particularly vulnerable to land-use 3.0 0.063 NS 0.4 0.661 NS 5.9 1.6 0.216 NS 39.5 55.7 conversion.

ﬂ ah

Complementarity fh

f a a ah

A few words of caution are needed when using the terms ﬂ gh fh

f a f h al

functional complementarity or redundancy regarding our gl al gl conclusions: functional diversity is always inherently deﬁ ned

g g g g l by the selection of traits (Hillebrand and Matthiessen 2009) and our deﬁ nition is rather broad. However, we justify this 0.029 0.017 0.001 0.001 0.001 0.001 by the fact that we did not aim at predicting changes in a

S single ecosystem function in response to land-use diﬀ erences

(Butterﬁ eld and Suding 2013), but that the combination of 3.9 4.8 10.9 13.8 46.6 21.0 a large amount of trait information in our study provides a robust measure of the overall functional distinctness of com-

2 munities (Winter et al. 2013). DF F p Effect F pSpecies Effect richness F is the p most commonly used indicator of diversity (Magurran 2004) and is still frequently dis- igh) for species richness (S), average taxonomic distinctness (Δ (S), average igh) for species richness h cussed as a proxy for functional diversity of communities (Milder et al. 2008, Larsen and Ormerod 2010). However, ow or ow l Naeem and Wright (2003) already suggested that the rela-

LU-intensity tionship between species richness and functional diversity

), trait richness (TR) and trait composition (TC) of Araneae, Carabidae and Heteroptera communities. Note that effect direction and Heteroptera Carabidae Araneae, composition (TC) of (TR) and trait richness ), trait

X of communities may be complex and context dependent

(Rader et al. in press). In our study, species richness was not CarabidaeHeteroptera 0.8 0.491 NS 0.6 0.554 NS 0.4 0.665 0.3 0.703 0.3 0.737 1.5 0.181 Residuals 30 Araneae CarabidaeHeteroptera Araneae CarabidaeHeteroptera 1.4 0.254 NS 0.5 0.485 NS 0.4 0.517 0.8 0.323 0.11 0.748 1.6 0.176 Araneae 0.1 0.714 NS 2.3 0.143 NS

X use intensity ( Table 4. Pseudo-F, p-values and effect direction from permutational analyses of variance of two-factorial models with the ﬁ of two-factorial and effect direction from permutational analyses of variance p-values 4. Pseudo-F, Table ( compositional measure and has no effect direction. Note that the residual DF for models with Δ is a multivariate, Land-use type 2 IntensityLU-type 1 sites. signiﬁ cantly related to the average functional distinctness

895 Figure 3. Median and 25 and 75 percentiles of the average functional distinctness ( X ) in high (open) and low (grey) intensity plots in forests, grasslands and arable fi elds for (a) Araneae, (c) Carabidae and (e) Heteroptera communities and average functional distinctness values corrected for taxonomic distinctness ( X ∼ Δ ) for (b) Araneae, (d) Carabidae and (f) Heteroptera communities. Note that N 4 for high intensity arable land plots instead of 6 in Heteroptera due to the presence of only a single species at two sites. of Araneae and Heteroptera communities. Only Carabidae ple, if a few closely related species are replaced by species that communities had a signifi cantly higher average functional have no close relatives in the community (see also Kessler distinctness in communities that also had higher species et al. 2009) or if functionally similar species are replaced by richness. Th is result suggests that a loss of species would have species with one or more exceptional traits (Mayfi eld et al. negative consequences for the average functional distinct- 2010). All analyzed arthropod taxa were characterized by a ness of Carabidae communities, but might be less critical higher functional distinctness in taxonomically more dis- for the functional distinctness of Araneae and Heteroptera tinct communities if analyzed independent of land-use type communities. Th e species richness of Carabidae communi- or intensity. Th is pattern suggests that, similar to a proposed ties was not signifi cantly aff ected by land-use intensity and relationships between phylogenetic diversity and functional Carabidae are known to be among the invertebrate taxa that diversity (Flynn et al. 2011 and references therein), adding a are less vulnerable to species loss by, for example, agricul- taxonomically distantly related species will also increase the tural intensifi cation (e.g. organic versus conventional farm- functional distinctness of communities. In contrast to spe- ing, Birkhofer et al. 2012) or increased forest management cies richness, we can assume that functional distinctness will intensity (Lange et al. 2014). A general loss of species and a decline if land-use change leads to a decline of taxonomic consequent loss of traits due to land-use intensifi cation, as distinctness in terrestrial arthropod communities. it is predicted by the sampling eff ect hypothesis (Mayfi eld et al. 2010), can therefore not be expected in any of the Functionality analyzed arthropod taxa in this study. However, changes in some aspects of biodiversity, such a community composition Intensive land use resulted in a lower average functional or functional diversity, do not necessarily mirror changes in distinctness of Araneae communities in managed grasslands richness (Purvis and Hector 2000). Species turnover can alter and of Heteroptera communities in managed grasslands the taxonomic or functional distinctness of communities and arable fi elds even after accounting for the taxonomic without changing the overall number of species. For exam- distinctness of communities. Th e opposite pattern of higher

896 Figure 4. Median and 25 and 75 percentiles of the rarifi ed trait richness in high (open) and low (grey) intensity plots in forests, grasslands and arable fi elds for (a) Araneae, (b) Carabidae and (c) Heteroptera communities. Note that N 4 for high intensity arable land plots instead of 6 in Heteroptera due to the presence of only a single species in two plots. Figure 5. Non-metric multidimensional scaling (NMDS) ordina- tion based on the proportional contribution of each trait variable at each site for (a) Araneae (2-d stress 0.08), (b) Carabidae (2-d functional distinctness under intensive land use was observed stress 0.05) and (c) Heteroptera (2-d stress 0.09) communities. in Araneae communities in arable fi elds and Heteroptera Araneae and Heteroptera communities are shown for low (open) communities in forest habitats. Th e fi rst observed pattern and high (closed) intensity sites in forests (᭡ ), grasslands (᭿ ) and resembles eff ects of land-use intensity on the functional arable fi elds (᭹ ) due to the signifi cant interaction term, Carabidae diversity in plants, mammals and birds and pollinator com- communities are only shown for the signifi cant land-use type term. munities (Flynn et al. 2009, Laliberté et al. 2010, Andersson Vectors are plotted for trait variables with multiple correlation coeffi cients 0.3. Th e circle stands for the maximum possible correla- et al. 2013, Birkhofer et al. 2014a). Th e common explana- tion coeffi cient (1.0). Traits are: Araneae: low or high ballooning tion for such eff ects is that intensive land use and the associ- propensity, active on the surface or vegetation layer, hunting with ated environmental stress leads to a reduction of available sheet-webs or cursorial, adults in summer and body length 1 0 niche-space (environmental fi ltering, D í az et al. 2013). Th e mm; Carabidae: macropterous or brachypterous, active in vegeta- niche fi ltering concept then suggests that this reduction of tion layer, carnivorous or phytophagous an body length 2– 7, 7– 12, niche space leads to functionally more narrow communi- 12 – 17 or 17 mm; Heteroptera: brachypterous, preferences for ties (Franzé n 2004, Statzner and Moss 2004; note that spe- shrub/tree stratum and carnivorous or mycetophagous adults. cies richness does not necessarily show this pattern, Gerisch et al. 2012). However, the dependency of this land-use eff ect niche-fi ltering eff ects on the functional distinctness of inver- on land-use type and arthropod taxon in our study should tebrate communities. Th is conclusion is further supported caution us towards a critical perception of the generality of by the fact that the rarifi ed trait richness in our study was

897 also not negatively aff ected by land-use intensity in a con- that species with poor mobility are more severely aff ected sistent manner. by anthropogenic disturbance than very mobile species, but Th e second observed pattern of higher functional distinct- that these results are often ambiguous (Smith et al. 2014). ness under more intense land use is more diffi cult to explain: Th e characteristic traits for Araneae and Carabidae commu- why are communities of Araneae (arable) and Heteroptera nities in forest communities compared to more frequently (forest) functionally more distinct and richer in traits under disturbed arable land and managed grasslands with several high land-use intensity? A combination of two explanations intra-annual disturbances (soil management, fertilization, may lead to such pattern: fi rst, our data does not include pesticide spraying and harvest) are large body sizes and low high nature value agricultural sites or pristine forests and dispersal ability (represented by large sheet-web weaving thus species with particular traits that are restricted to such Araneae species, Callobius claustrarius , Coelotes terrestris or habitats might not increase the functional distinctness at our Inermocoelotes inermis or large brachypterous Carabidae spe- low intensity sites. Both, invertebrate communities in forests cies from the genus Carabus , Abax parallelepipedus or Molops and arable land can include species that may be exclusively elatus) and these traits would be threatened if forest areas are observed under very low land-use intensity and these spe- converted to grasslands or arable land. cies are often of conservation value. Araneae communities in arable fi elds for example suff er from intense soil management (Th orbek and Bilde 2004) and species that prefer to Conclusions live under stones or in cracks in the soil particularly benefi t from the absence of tillage practices (Birkhofer et al. 2014b). Our results suggest that species loss will not generally lead Second, disturbance caused by land-use intensifi cation can to a lower functional distinctness in terrestrial arthro- increase the species richness in communities by favoring spe- pod communities, but that a reduction in the taxonomic cies and traits that were previously not present in a commu- distinctness of communities will lead to a loss of functional nity. Araneae or Carabidae communities have species groups distinctness. We further conclude that niche fi ltering might that are characterized by higher species richness under more cause lower functional distinctness at high intensity sites or intense agricultural management in arable land (Birkhofer in more frequently disturbed land-use types in some cases, et al. 2012, 2014a). In forests, coniferous trees and indicator but cause higher functional distinctness in other cases. Th is species for disturbance among herbacous plants are favored context dependency suggests that there is no general eff ect under high management intensity (Boch et al. 2013), which of environmental fi ltering on the functional distinctness promotes associated Heteroptera species with traits being of terrestrial arthropod communities. Our analysis of absent from communities in low intensity plots (e.g. spe- trait composition shows that particular traits show shared cies with specifi c phenological and feeding traits on spruce; responses to land-use types between diff erent taxa (e.g. higher Gossner 2008). dominance of large species in forest systems for Araneae and Araneae and Heteroptera communities were functionally Carabidae communities), but that the opposite pattern can most distinct in forests, but Carabidae showed the opposite also be observed (e.g. higher dominance of species with low pattern. Th e more permanent and structurally richer nature dispersal ability for Araneae and Carabidae communities, of forests may have contributed to the higher average func- but with high dispersal ability for Heteroptera communi- tional distinctness of Araneae and Heteroptera communities ties in forest systems). We argue that future studies with a in forests. Th e trait composition further separated communi- focus on eff ects of anthropogenic disturbances on terrestrial ties in forests from communities in grasslands or arable fi elds arthropod communities should account for the relatedness for all three taxa, whereas a comparable level of separation between species and the functional diversity of communities. between grasslands and arable fi elds was only evident for In addition, studies need to link changes of functional diver- Araneae communities. Th e identifi cation of traits that are sity in arthropod communities due to land-use change to characteristic for land-use types or intensity levels provides ecosystem functions. Only such comprehensive approaches insights about threats for particular traits if land use is inten- will provide a more mechanistic understanding of the sifi ed or if land-use types would be converted. Our results relationship between anthropogenic changes and biologi- meet the expectations based on general ecological knowl- cal communities, which is crucial to develop strategies for edge: losers of land-use conversion from relatively undis- the simultaneous conservations of species diversity and turbed forests to more frequently disturbed arable fi elds are ecosystem functionality. large species with low to intermediate dispersal capabilities (Araneae and Carabidae), or carnivorous species (Carabidae Acknowledgements – We thank the subject editor for comments that and Heteroptera). Land-use intensity further aff ected the improved an earlier version of the manuscript. We are grateful to all trait composition in Heteroptera communities, suggest- colleagues and students that helped with data collection and Th eo ing that brachypterous species benefi t from lower land-use Blick for trait information on spiders. We are further grateful to the intensity in all land-use types. It has long been argued that manager of the exploratory Hainich, S. Gockel for her work in community responses to disturbance may be best assessed maintaining the plot and project infrastructure; S. Pfeiff er and C. by using body size or body mass changes (Saint-Germain Fischer giving support through the central offi ce, and M. Fischer, K. E. Linsenmair, D. Hessenm ö ller, J. Nieschulze, D. Prati, I. et al. 2007). Th e rationale is that smaller species may sur- Schö ning, F. Buscot, E.-D. Schulze and the late E. Kalko for their vive management-induced disturbances, due to the fact that role in setting up the Biodiversity Exploratories project. Th e work these species can hide or escape (Postma-Blaauw et al. 2010) has partly been funded by the DFG Priority Program 1374 and can often re-colonize disturbed areas faster due to a ‘ Infrastructure-Biodiversity-Exploratories ’ (WE 2618/9-1; WE higher mobility (Birkhofer et al. 2013). It has been suggested 3081/21-1). Field work permits were issued by the responsible state

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Supplementary material (Appendix ECOG-01141 at www.ecography.org/readers/appendix ). Appendix 1 – 4.

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