Effects of forest management on ground-dwelling beetles (Coleoptera; Carabidae, Staphylinidae) in Central Europe are mainly mediated by changes in forest structure

Forest Ecology and Management 329 (2014) 166–176

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Effects of forest management on ground-dwelling beetles (Coleoptera; Carabidae, Staphylinidae) in Central Europe are mainly mediated by changes in forest structure Markus Lange a,b,⇑, Manfred Türke a,c, Esther Pašalic´ a, Steffen Boch d, Dominik Hessenmöller b, Jörg Müller e, Daniel Prati d, Stephanie A. Socher d, Markus Fischer d, Wolfgang W. Weisser a,c, Martin M. Gossner a,c a

Institute of Ecology, Dornburger Str. 159, Friedrich-Schiller-University Jena, 07743 Jena, Germany Max-Planck-Institute for Biogeochemistry, Hans-Knoell-Str. 10, 07745 Jena, Germany c Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising-Weihenstephan, Germany d University of Bern, Institute of Plant Sciences, Altenbergrain 21, CH-3013 Bern, Switzerland e Institute of Biochemistry and Biology, University of Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany b

a r t i c l e

i n f o

Article history: Received 28 February 2014 Received in revised form 31 May 2014 Accepted 4 June 2014

Keywords: Beech forest Biodiversity Exploratories Conifer plantations Habitat preferences Insects Land use

a b s t r a c t Forest management is known to influence species diversity of various taxa but inconsistent or even contrasting effects are reported for arthropods. Regional differences in management as well as differences in regional species pools might be responsible for these inconsistencies, but, inter-regional replicated studies that account for regional variability are rare. We investigated the effect of forest type on the abundance, diversity, community structure and composition of two important ground-dwelling beetle families, Carabidae and Staphylinidae, in 149 forest stands distributed over three regions in Germany. In particular we focused on recent forestry history, stand age and dominant tree species, in addition to a number of environmental descriptors. Overall management effects on beetle communities were small and mainly mediated by structural habitat parameters such as the cover of forest canopy or the plant diversity on forest stands. The general response of both beetle taxa to forest management was similar in all regions: abundance and species richness of beetles was higher in older than in younger stands and species richness was lower in unmanaged than in managed stands. The abundance ratio of forest species-to-open habitat species differed between regions, but generally increased from young to old stands, from coniferous to deciduous stands and from managed to unmanaged stands. The response of both beetle families to dominant tree species was variable among regions and staphylinid richness varied in the response to recent forestry history. Our results suggest that current forest management practices change the composition of ground-dwelling beetle communities mainly by favoring generalists and open habitat species. To protect important forest beetle communities and thus the ecosystem functions and services provided by them, we suggest to shelter remaining ancient forests and to develop near-to-nature management strategies by prolonging rotation periods and increasing structural diversity of managed forests. Possible geographic variations in the response of beetle communities need to be considered in conservation-orientated forest management strategies. Ó 2014 Elsevier B.V. All rights reserved.

1. Introduction Land-use intensification and change are major drivers of biodiversity loss (e.g. Sala et al., 2000). This is particularly true for forest ⇑ Corresponding author. Present address: Max-Planck-Institute for Biogeochemistry, Hans-Knoell-Str. 10, 07745 Jena, Germany. Tel.: +49 3641 576168. E-mail address: [email protected] (M. Lange). http://dx.doi.org/10.1016/j.foreco.2014.06.012 0378-1127/Ó 2014 Elsevier B.V. All rights reserved.

ecosystems, which harbor a high proportion of global biodiversity. In temperate forests, novel management systems have been developed during the last century to fulfill the increasing demands for timber. But recent forest management may conflict with recent biodiversity conservation purposes. For instance, natural beech forests have been largely converted into coniferous plantations in Central Europe or have become the subject of increasing management intensification by reducing rotation periods (Hannah et al.,

M. Lange et al. / Forest Ecology and Management 329 (2014) 166–176

1995). As a consequence, ancient temperate broadleaf forests with long-lasting habitat continuity of more than 200 years have become rarer and are a conservation priority (Peterken, 1981; Goldberg et al., 2007; Fritz et al., 2008). As a result of forest management a decrease in species richness has been shown for various taxonomic groups such as Carabids and saproxylic beetles (Paillet et al., 2010; Buse, 2012). Although an increasing effort has been made in the past years to reconcile economic and ecological issues (Spiecker, 2003; Ammer et al., 2008; Boncina, 2011), the capacity of current forest practices to maintain forest species is still unclear (Niemelä et al., 2007; Gossner et al., 2013). Arthropods are the most diverse animal group in all terrestrial ecosystems and are known to play an important role for ecosystem functioning (Weisser and Siemann, 2004) and ecosystem services (Prather et al., 2013). For several arthropod groups, including different functional groups such as predators and wood decomposers, there is a clear indication that they are negatively affected by forest management (Niemelä et al., 2007; Gossner et al., 2013). Carabid and staphylinid beetles comprise a number of feeding habits, but the majority of species are considered generalist predators (Lövei and Sunderland, 1996). As such they have been assumed to be effective biocontrol agents (Kromp, 1999; Symondson et al., 2002), e.g. the forest caterpillar hunters of the Carabid genus Calosoma (Weseloh, 1985; Weseloh et al., 1995; Alalouni et al., 2013) but their role in regulating pest populations is not completely clear (Koivula, 2011; Alalouni et al., 2013). Moreover, ground-dwelling beetles affect several ecosystem processes, e.g. as mediators of nutrient flows (Loreau, 1995). Staphylinid and carabid beetles are sensitive to changes in their environment, and react quickly to increasing forest management intensity (Thiele, 1977; Niemelä and Halme, 1992; Baguette, 1993; Luff, 1996). Thus, their potentially important role as predators might be undermined by changes in forest management. Moreover, species composition may well reflect forestry history (Assmann, 1999; Finch, 2005). As such, they have been recommended as indicator groups of forest management intensity (e.g. Buse and Good, 1993; Butterfield et al., 1995; Pohl et al., 2007) and suggested to be included in conservation and restoration efforts (Schowalter, 2006). Forest management may influence arthropod communities either directly by reducing population size during harvest activities or indirectly by affecting habitat availability (shelter, overwinter structures), habitat heterogeneity, or prey availability. In particular, the complete replacement of dominant tree species by another, more economically viable species, is one of the most severe habitat changes caused by forest management (Brunet et al., 2010). In Central Europe, beech forests have largely been replaced by conifers, in particular spruce or pine forests, and additionally transferred from forests with high structural diversity into single layered plantations. According to Hannah et al. (1995), 82% of Central European forests are human dominated (highly disturbed). In addition to these changes related to tree species composition, forest habitat quality and structural heterogeneity has been reduced in many forests due to intensified age-class forestry. These even-aged forests are low in structural diversity and thus, exhibit a lack of important resources for many species such as old trees, early phases of natural succession and, above all, large-sized dead trees and their continuous availability in forests (Bauhus et al., 2009; Meyer and Schmidt, 2011). These factors hold negative consequences for those species that do not directly depend on the trees themselves, such as generalist insect predators (Niemelä et al., 1993; Koivula, 2002; Finch, 2005; Barsoum et al., 2014). For ground-dwelling predators a negative effect of these structural changes caused by forest management can be expected, for example, due to reduced plant diversity. The ‘enemies hypothesis’ (Root, 1973; Russell, 1989) predicts lower predator abundance

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and diversity with decreasing plant diversity due to reduced niche diversity and resource availability. The ‘enemies hypothesis’ is, however, not supported by all studies on ground-dwelling predators in forests as recently reported by Schuldt et al. (2011). Another important question is, if changing the dominant tree species or increasing forest management intensity (e.g. from unmanaged to managed uneven-aged to managed even-aged forests) while still maintaining the dominant tree species, has more severe consequences for ground beetle communities. And furthermore, which structural changes caused by these two components of forest management drive community changes. Negative effects of forest management on ground-dwelling arthropods have not generally been identified. Allegro and Sciaky (2003) studying poplar stands and natural woods in Italy, and Fuller et al. (2008) comparing coniferous and broadleaved forests in the UK, for instance, found no difference in carabid species richness between managed and unmanaged forests. Villa-Castillo and Wagner (2002) even found higher diversity in managed compared to unmanaged forests in northern Arizona. These contrasting findings might be a result of regional differences, as most studies focus on a single group in a single region only (e.g. Pohl et al., 2007; Fuller et al., 2008), but see Barsoum et al. (2014). Regional differences in habitat preferences are known for many ground-dwelling species (Gossner et al., 2014). Thus, studies in different regions are challenging to test for more general consequences of forest management on ground-dwelling species diversity (Koivula, 2012). In contrast to species richness, community composition differed between forest types in most studies, mainly due to a change from specialized forest species to habitat generalists e.g. (Allegro and Sciaky, 2003; Fuller et al., 2008) suggesting a more general consequence of forest management. In this study we investigated the influence and quantified the relative importance of forest management and environmental characteristics on ground dwelling beetle communities with special attention to geographic variation in responses. Forest management was determined by differences among forest types, comprising differences in recent forestry history (managed vs. unmanaged). Within managed stands we contrasted beech stands and coniferous plantations. We further distinguished between stands of young and old developmental stages within even-aged forestry. Studying three regions differing in climate, geology and topography enabled us to generalize our findings. We addressed the following questions: (1) do differences in dominant tree species (beech, oak, spruce, mixed), stand age (young or old) and recent forestry history affect abundance, species richness and composition of beetle communities and are effects similar across regions?, (2) are effects of forest management on beetle communities mediated by environmental characteristics and what is their relative importance?, and (3) does the composition of both families of ground-dwelling beetles similarly reflect recent forestry history?

2. Materials and methods 2.1. Study regions The study was conducted in three different geographical regions in Germany within the framework of the BiodiversityExploratories Project (http://www.biodiversity-exploratories.de), the Schorfheide-Chorin in the North–East (52° 470 24.800 to 53° 130 26.000 N; 13° 230 2700 to 14° 80 52.700 E), the Hainich-Duen in the Center (50° 560 14.500 to 8 51° 220 43.400 N; 10° 100 24.000 to 10° 460 45.000 E) and the Schwaebische Alb in the South-West (48° 200 60.000 to 48° 320 3.700 N; 9° 120 13.000 to 9° 340 48.900 E). The three regions differ in geographical characteristics, e.g. altitude

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increases from the Schorfheide-Chorin (3–140 m a.s.l.) towards the Hainich-Duen (285–550 m) and further to the Schwaebische Alb (460–860 m). Soil types in the Schorfheide-Chorin are mainly Cambisols, in the Hainich-Duen Luvisols and Stagnosols and in the Schwaebische Alb Cambisols and Leptosols. While mean annual temperature decreases from the Schorfheide-Chorin (8–8.5 °C) to the Hainich-Duen (6.5–8 °C) to the Schwaebische Alb (6–7 °C), precipitation is lowest in the Schorfheide-Chorin (500–600 mm) and increases towards the Hainich-Duen region (500–800 mm) and the Schwaebische Alb (700–1000 mm) (Fig. 1; Fischer et al., 2010). 2.2. Study sites and forest types In our study 50 experimental plots (EP) of 100 m  100 m were selected by a stratified random design in each of the three regions. From about 500 candidate sites representing major forest types per region, 50 one-hectare forest plots were selected representing a similar range of management intensities on the typical soils in the region (Schwaebische Alb: Cambisol/Leptosol; Hainch-Duen: Luvisol/Stagnosol; Schorfheide-Chorin: Cambisol) (Fischer et al., 2010). A number of additional criteria were employed for plot selection, e.g., a distance of at least 200 m between the borders of each plot. The stratified random selection of plots was also used to reduce spatial autocorrelation. Forest types comprise unmanaged deciduous, European beech-dominated stands (Fagus sylvatica L.) (unmanaged since 20–70 years) and even-aged forest stands (age-class forestry) of different developmental stages. These even-aged stands were either deciduous (dominated by European beech F. sylvatica) or coniferous (dominated by Norway spruce

(Picea abies (L.) H. Karst.) in the Schwaebische Alb and the Hainich-Duen and by Scots Pine (Pinus sylvestris L.) in the Schorfheide-Chorin). The trees of even-aged stands belong to more or less confined age cohorts and are harvested at 60–80 (coniferous plantations) up to 120 (deciduous stands) year intervals. Due to a low number of replications in each development stage of even-aged stands, as they are commonly considered in forestry, we pooled stands with a diameter at breast height (DBH) < 15 cm as ‘young even-aged’ (termed ‘thicket’ and ‘pole wood’ in age-class forestry) and all stages with trees >15 cm DBH as ‘old even-aged’ (termed ‘young and old timber stage’ in age-class forestry). We additionally accounted for regional distinctions of forest type, by including even-aged forests of sessile oak (Quercus petraea (Mattuschka) Liebl.) and mixed pine-beech forests in the Schorfheide-Chorin and uneven-aged beech dominated stands, in which single or small groups of trees are harvested selectively, in the Hainich-Duen. 2.3. Beetle sampling and measuring their community We used pitfall traps to sample ground-dwelling arthropods (funnel traps with a diameter of 15 cm; see Lange et al. (2011a) for general design). We installed three pitfall traps per experimental plot, one in each of three randomly selected corners. As sampling fluid we used copper-sulfate solution (3%) and added a drop of detergent to reduce surface tension. During the entire growing season from mid of April to mid of October 2008 we emptied traps five times in an interval of five to six weeks. We transferred arthropods into 70% ethanol in the field and subsequently sorted to taxonomic orders in the laboratory. Due to trap losses we randomly selected two out of three undamaged traps per plot independently for each sampling interval. We pooled all data for each plot and across all five sampling intervals, resulting in a total of 149 sample units (Schorfheide-Chorin 50, Hainich-Duen 49, Schwaebische Alb 50). We focused on ground beetles (Carabidae) and rove beetles (Staphylinidae). Taxonomic specialists recruited for the project identified carabids and staphylinids to species level, based on Freude et al. (1965–83). All beetle individuals are stored at the Technische Universität München. All carabid and staphylinid species were classified according to their habitat preferences based on Koch (1989–95). We grouped species into forest species, open habitat species, remaining wet habitat species, and habitat generalists that are ubiquitous (see Appendix Table A.1). If species prefer wet forests or wet open habitats, they were assigned to forest species or open habitat species, respectively. Wet habitats species without more detailed information on habitat type were not analyzed separately in their response to different forest types (in average, they account for less than 1.5% of all species per trap). Furthermore, we classified all species in feeding guilds (herbivores, carnivores, mycetophages, saprophages) according to their main food source. Classification was based on Koch (1989–95) and Böhme (2005). 2.4. Environmental variables

Fig. 1. Geographic location of the three Biodiversity Exploratories within Germany (adapted from Fischer et al., 2010).

A forest inventory was performed in the core area of each plot (Hessenmöller et al., 2011). Within concentric circles with a radius of 12.62 m the position of all trees (>7 cm DBH) was determined by distance and direction and the tree species, DBH and tree height was noted. Furthermore, basal area (m2/ha), coarse woody debris (length >0.5 m and diameter >0.2 m, m3/ha) and fine woody debris (diameter >0.05 m, m3/ha), quantile 90 of tree height (m) and solid volume (>7 cm in diameter, m3/ha) were measured. Soil types were determined in a soil inventory (Fischer et al., 2010) and described according to the World Reference Base of Soil Resources (IUSS Working Group WRB 2006).

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On each plot we conducted a forest vegetation survey on a 20 m  20 m subplot at the forest inventory circle in spring and summer, in order to record both early spring geophytes and later emerging species (Boch et al., 2013). We identified all vascular plant species and estimated the percentage cover per species separately for the herb, shrub and tree layers. To assess the total number of vascular plants per plot, we combined the spring and summer records for all species. In addition, we calculated the Shannon diversity. As further structural parameters we estimated the cover of litter and bare soil. A total of 30 environmental variables were considered in our analyses (Table A.1).

and unmanaged beech stands (Model 2: Hainich-Duen, N = 45; Table 1b). For the Schorfheide-Chorin, we tested for differences among the following forest types: old even-aged stands of mixed pine-beech, old oak stands, old even-aged beech stands and old even-aged pine stands and unmanaged beech stands (Model 3: SchorfheideChorin, N = 39 stands, Table 1c). Furthermore, we applied non-metric multidimensional scaling (NMDS) (‘metaMDS’-function implemented in the vegan package) to compare the community composition of ground-dwelling beetles among all forest types. To detect shifts in the community composition we used two-dimensional NMDS. We used relative abundance data of species (Bray–Curtis distance) rather than presence–absence data because relative abundances are important determinants of community structure. In addition, we performed a Permutational Multivariate Analysis of Variance (PERMANOVA) to test whether there is a significant difference between community composition of different forest types (‘adonis’-function in vegan package, permutations = 999). In the PERMANOVA, the different forest types were nested within regions.

2.5. Data analysis We conducted all analyses in R 3.0.1 (R Development Core Team, 2013). In a first step we investigated differences of the focal taxa communities among different forest types (question 1). We used the term ‘‘community structure’’ for describing abundance, species richness and abundance ratios of species associated with different habitats. We use ‘‘community composition’’ when considering all individuals in multivariate approaches.

2.5.2. Analyses on the relative importance of forest types and environmental factors The second step of our analyses was intended to identify if effects of different forest types on beetle communities were mediated by environmental variables and to quantify the relative importance of forest types and environmental characteristics among different regions (question 2). Similar to the procedure in Loranger et al. (2012) we used the random forest approach (‘randomForest’-function implemented in the MASS package) to identify the ten most important environmental variables out of all 30 variables considered here (see Section 2.4, Table A.2). In short, random forest uses series of regression trees to derive importance scores that indicate the most important environmental variables for predicting means of the community structure among a large number of variables (see Tables A.3 for detailed results of the random forests selection). A priori we fitted first the 10 most important variables in ANCOVAs, in a sequence according to their importance (Table A.3), followed by all categorical variables of forest types and region. In the next step we did a stepwise model simplification in both directions (backward and forward, starting with the full model), based on the Akaike information criterion (AIC). Furthermore, we used variance partitioning to quantify the relative contribution of forest types, environment characteristics and region to the entire beetle community composition (‘varpart’-function in vegan package).

2.5.1. Analyses on the forest types effect To test for general management effects we applied an ANOVA comprising all regions and all forest types that occurred in at least two regions (Model 1: inter-regional, N = 118; Table 1a). We fitted first Region (Schorfheide-Chorin, Hainich-Duen, and Schwaebische Alb) to control for regional differences in beetle communities. To separate between effects of recent forestry history, dominant tree species and stand age we applied a hierarchical model framework; first we tested for differences between managed and unmanaged stands, secondly within managed stands we tested for differences between even-aged coniferous and even-aged beech stands, and finally within even-aged beech stands we tested for differences between young and old developmental stages (Table 1a and Table A.2). In addition, we included interaction terms of region and management variables to test for differences in management effects among regions. The inter-regional model had the following specification: aov (y  region  recent forestry history + region  dominant tree species + region  stand age). All variables used in this model are categorical (Table A.2). To test for effects of forest types occurring only in a single region, we used One-Way-ANOVAs, followed by Tukey’s HSD post hoc tests (a = 0.05). For the Hainich-Duen region we tested for differences among the following forest types: uneven-aged beech stands, young even-aged beech stands, old even-aged beech stands

Table 1 Number of plots of each forest type used for the three ANOVAs (inter-regional, Hainich-Duen, Schorfheide-Chorin) in order to consider regional differences in forest management. Recent forest history

Managed (even-aged)

Dominant tree species

Conifera

Pine-beechb

Beechb

Stand age

Old

Old

Young

Old

(a) Model 1: inter regional SchwaebischeAlb Hainich-Duen Schorfheide-Chorin Sum

12 4 12 28

15 9 0 24

18 11 14 43

9

11

(b) Model 2: Hainich-Duen Beech stands (c) Model 3: Schorfheide-Chorin Timber stands 12 a b c

6

7

Managed (uneven-aged)

Unmanaged

Oakc

Beechb

Beechb

Old

Uneven

Uneven

13 7

Sum

5 12 7 24

50 36 33 118

12

45

7

39

Coniferous stands were either dominated by Norway spruce Picea abies (Schwaebische Alb, Hainich-Duen) or by Scots pine Pinus sylvestris (Schorfheide-Chorin). European beech Fagus sylvatica. Sessile oak Quercus petraea.

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We log transformed abundance data and the ratio of carabid habitat types and square root transformed ratio of staphylinid habitat to obtain normal distributed error structure and to stabilize the variances. 3. Results In total we caught 109,677 individuals of 429 species of grounddwelling carabids and staphylinids. Although the abundance of carabids (77,701 individuals) was more than twice the number of staphylinids (31,976), the species richness of carabids (108 species) was lower than that of staphylinids (321 species) (Table 2). In both beetle families the majority of sampled individuals and species were predators; in carabids 98.3% of individuals and 77.8% of species, and in staphylinids 92.6% of individuals and 86.9% of species. While the remaining carabids were herbivores (N = 1316; S = 24), in staphylinids only a few herbivores occurred (N = 13, S = 5). Other staphylinids were either mycetophages (N = 372, S = 10) or saprophages (N = 1969, S = 27). 3.1. Inter-regional effects of forest types on community structure 3.1.1. Abundance and species richness The inter-regional model (Table 1) explained 30% and 54% of the variance regarding the abundance of carabids and staphylinids, respectively. The main portion of this variation was covered by the region. Carabid abundance decreased from the SchorfheideChorin region in the North–East towards the Schwaebische Alb region in the South–West, while in staphylinids this trend was opposite (Tables 2 and 3). There was no difference between managed and unmanaged forests in the abundance of both groups. We observed higher carabid abundances in coniferous than in beech stands of the Schwaebische Alb (Fig. 2), while we found no difference in the other regions (significant interaction ‘regionby-dominant tree species’; Table 3). The abundances of staphylinids was lower in coniferous than in beech stands. The abundances of both beetle families were significantly higher in older than in younger stages of even-aged forests. However, the effect of stand age on staphylinid abundances was only significantly different in the Schwaebische Alb as indicated by the significant interaction term ‘region-by-stand age’ (Fig. 2). Similar to abundance, the variance of beetle richness explained by the inter-regional model was much lower in carabids (23%) than staphylinids (67%) and similar to abundances, most of the variation was explained by region (Table 3). In both beetle families, most species were found in the Schorfheide-Chorin, followed by Hainich-Duen and Schwaebische Alb (Table 2). Overall, the richness of carabids was significantly higher in managed than in unmanaged stands, while the recent forestry history showed no clear effect on staphylinid richness across regions. Furthermore, staphylinid and carabid richness was not affected by whether the stands were coniferous or

deciduous, i.e. beech stands. Overall, old deciduous even-aged stands were more diverse in carabids and staphylinid species than young ones (Fig. 2). 3.1.2. Habitat associated species In all regions and all forest types, communities were dominated by forest species but the proportion of these species varied considerably, ranging from 66% to 97% of all species (Table 2). Restricting analyses in the inter-regional model to forest species (Table A.4), abundance of forest carabids was not affected by recent forestry history and dominant tree species, while we found more forest carabids in old than in young stands (F2,107 = 20.13; p < 0.001). Forest staphylinids were more abundant in deciduous stands than in coniferous stands (F2,107 = 6.20; p = 0.014) and in older than in younger stands (F2,107 = 32.28; p < 0.01). Forest carabids were richer in species in older stands than in younger ones and did not respond to recent forestry history and dominant species. Richness of forest staphylinids did not respond to different forest types. The abundance-ratio of forest-to-open habitat species of carabids as well as of staphylinids, differed significantly among regions; it increased strongly from the Schorfheide-Chorin region to the Hainich-Duen and further to the Schwaebische Alb (Table 3, Fig. 2). The abundance-ratio of carabid beetles responded to recent forestry history, but not equally among all three regions, indicated by the significant interaction terms region-by-recent forestry history. In the Schorfheide-Chorin and Schwaebische Alb the ratio was higher in recently unmanaged than managed stands, while in the Hainich-Duen region the ratio was higher in managed stands. The effect of dominant tree species on the carabid ratio was not consistent, too, as the ratio was higher in coniferous stands in the Schwaebische Alb and Hainich-Duen region, but not in the Schorfheide-Chorin region. The abundance-ratio of staphylinid forest species-to-open habitat species was generally higher in recently unmanaged than in managed stands, higher in deciduous than in coniferous stands and higher in old deciduous than in young deciduous stands (Table 3, Fig. 2). 3.2. Regional distinct forest types Considering the forest types occurring only in one region, both beetle groups differed neither in abundance or species richness nor in the ratio of forest-to-open habitat species between uneven-aged forests (Hainich-Duen region) and young or old even-aged beech stands and unmanaged beech forests (Table A.5). In the Schorfheide-Chorin, abundance, richness and the ratio of forest-to-open habitat species did not differ between forest types, i.e. even-aged mixed stands of beech and pine and the even-aged stands of oak compared to other forest types (Table A.5). The only exception was the significantly higher staphylinid abundance in oak stands compared to pine stands (Tukey post hoc test: p = 0.024).

Table 2 Mean (±SE) abundance, species richness and community structure of carabid and staphylinid beetles caught on all forest plots. The community structure is represented by the relative abundances of the habitat guilds (generalists, forest and open habitat species). Abundance

Species richness

Community structure (habitat guilds) Forest species

Generalists

Open habitat species

Carabidae SchwaebischeAlb Hainich-Duen Schorfheide-Chorin

651.12 (40.85) 492.39 (48.60) 471.76 (39.40)

18.92 (0.44) 19.00 (0.47) 21.26 (0.62)

0.97 (0.01) 0.90 (0.01) 0.82 (0.02)

0.02 (0.01) 0.04 (0.01) 0.07 (0.01)

0.01 (0.00) 0.06 (0.01) 0.07 (0.02)

Staphylindae SchwaebischeAlb Hainich-Duen Schorfheide-Chorin

160.16 (11.26) 157.42 (9.25) 330.88 (25.38)

22.12 (0.93) 26.22 (0.86) 44.02 (1.26)

0.86 (0.01) 0.83 (0.02) 0.66 (0.03)

0.11 (0.01) 0.14 (0.01) 0.27 (0.02)

0.00 (0.00) 0.01 (0.00) 0.02 (0.00)

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Table 3 Results of an ANOVA and ANCOVA comparing community structure (abundance, species richness, ratio of forest species-to-open habitat species) of carabid and staphylind beetles in different forest types in three regions. Bold text indicates significant effects (a = 0.05). Additionally, important environmental variables (see Tables A.2 and A.3) were fitted first, according to their importance. Stepwise model simplification (based on Akaike information criterion AIC) was performed. Letters indicate the sequence of variable exclusion from the full model, (starting with ‘a’). Letters combined with a ‘+’ indicate when an already excluded variable was included into the model again. Canopy refers to tree layer > 10 m, sub-canopy refers to tree layer 5–10 m. An additional correlation matrix for all continuous environmental variables is provided in Table A.10. Carabidae

Staphylinidae ANOVA F

Abundance Cover litter cover canopy Richness herbs Richness vascular plants Shannon Basal area Cover canopy & sub-canopy Shannon herbs Solid volume Mean arithmetic diameter Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age Species richness Cover sub-canopy Cover canopy & sub-canopy Tree height Shannon herbs Cover canopy Shannon Richness vascular plants Richness shrubs Solid volume Cover litter Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age Forest-to-open habitat species Soil type Richness vascular plants Cover bare soil Cover litter Richness herbs Cover canopy & sub-canopy Cover herbs Shannon Number trees Tree height Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age

7.38 1.19 0.00 19.11 0.69 4.64 0.51

4.38 11.88 2.03 6.36 0.43 0.57 1.39

82.72 0.16 1.82 1.28 9.33 4.63 0.20

ANCOVA P

F

0.001 n.s. n.s. 0.000 n.s. 0.012 n.s.

j 19.75 e f a g b c h i 9.17 0.67 0.87 7.89 0.77 6.42 d

0.015 0.001 n.s. 0.013 n.s. n.s. n.s.

e l g 5.72 a j f d k i 10.61 7.66 h 7.89 c b m

0.000 n.s. n.s. n.s. 0.000 0.012 n.s.

a b 10.02 f g i 17.18 h 27.29 e 75.26 0.01 0.93 d 12.86 5.37 c

ANOVA P

0.000

0.000 n.s. n.s. 0.006 n.s. 0.002

0.018

0.000 0.007 0.006

0.002

0.000 0.000 0.000 n.s n.s 0.000 0.006

3.3. Effects of forest types on community composition among regions Forest management significantly influenced the community composition of carabid and staphylinid beetles (NMDS, followed by a PERMANOVA; Table 4, Fig. 3a and b). The variation within the carabid community was explained by recent forestry history (3.5% of variation), stand age (4.7%) and mainly by the dominant tree species (5.6%; Table 4). Differences in the staphylinid community composition were mainly explained by the dominant tree

F Mean arithmetic diameter Tree height Mean quadratic diameter Shannon Soil type Richness sub-canopy Richness vascular plants Cover shrubs Richness herbs cover herbs Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age Shannon Richness herbs Cover canopy & sub-canopy Richness vascular plants Cover herbs Mean arithmetic diameter Cover litter Mean quadratic diameter Cover canopy Coarse woody debris Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age Cover litter Shannon Richness herbs Richness vascular plants Cover canopy & sub-canopy Cover canopy Shannon herbs Cover herbs Richness shrubs Number trees Region Forestry history Dominant tree species Stand age Region  forestry history Region  tree species Region  stand age

38.26 1.86 1.79 33.05 0.09 3.70 6.80

95.42 2.93 2.58 3.90 3.74 6.11 0.13

16.84 5.72 9.10 22.10 1.26 1.33 5.21

ANCOVA P

F

0.000 n.s. n.s. 0.000 n.s. 0.028 0.010

e k d h a 39.97 (g +) 18.50 0.01 b c 18.11 j 6.42 17.74 i f 8.34

0.000 0.090 n.s. 0.051 0.027 0.003 n.s.

48.40 b e h c g d f 9.53 3.56 72.82 1.24 1.79 8.18 4.04 6.43 a

0.000 0.019 0.003 0.000 n.s. n.s. n.s.

a k c d g f b i j e 16.79 5.70 9.08 22.04 1.26 h 5.51

P

0.000 0.000 n.s.

0.000 0.013 0.000

0.005 0.000

0.003 0.062 0.000 n.s. n.s. 0.005 0.020 0.002

0.000 0.019 0.003 0.000 n.s. 0.021

species (10.1%). Although recent forestry history and stand age have a significant effect on the staphylinid community composition, the explained variation was low (2.0%/2.6%). We found a high dissimilarity in beetle community compositions among regions (carabids: 9%; staphylinids 10% of explained variation), with most distinct communities found in the Schorfheide-Chorin region (Fig. 3a and b). These findings were underpinned by the number of species found exclusively in a single region. In SchorfheideChorin 41 carabid species (total S = 80) and 105 staphylinid species

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Fig. 2. Abundance (N) and species richness (S) and abundance ratio of forest-to-open habitat species of carabid and staphylinid beetles in different regions (Schwaebische Alb, Hainich-Duen, Schorfheide-Chorin) and forest types (coniferous even-aged (old), beech even-aged (young), beech even-aged (old), unmanaged forests). Results are based on data used in model 1 (N = 118 stands). Please note different y-axes scaling between abundance and abundance ratio graphs for both beetle families.

Table 4 Results of a Permutational Multivariate Analysis (PERMANOVA), based on distance matrices (Bray–Curtis) of carabid and staphylind community composition (relative abundances) and different forest types. Forest sites were nested within region. In the same PERMANOVA we also included regional distinct forest types (uneven-aged forest in the Hainich-Duen region (HAI) and oak stands and mixed beech-pine stand in the Schorfheide-Chorin (SCH)) and contrasted the beetle community compositions to the other forest types of the respective region. Bold text indicates significant effects (a = 0.05). Df

Recent forestry history Dominant tree species Stand age Uneven-aged (HAI) Oak (SCH) Mixed beech-pine (SCH) Coniferous young (SCH) Tree species  mixed beech-pine Residuals

1 1 1 1 1 1 1 1 140

Carabidae

Staphylinidae

F

P

R2

F

P

R2

6.73 10.63 8.95 2.20 9.95 4.90 5.87 1.06

0.001 0.001 0.001 0.865 0.004 0.124 0.206 0.200

0.035 0.056 0.047 0.012 0.052 0.026 0.031 0.006 0.739

3.66 18.40 4.77 2.98 4.13 3.20 3.67 0.89

0.002 0.001 0.004 0.700 0.323 0.182 0.272 0.502

0.020 0.101 0.026 0.016 0.023 0.018 0.020 0.005 0.771

(total S = 239) were found exclusively (Table A.6), which is about half of all species recorded in this region. In Hainich-Duen eight carabid (total S = 59) and 38 staphylinid species (total S = 174) were restricted to this region, corresponding to 17% and 22% of the all species in this region, respectively. Five carabid (total S = 50) and 27 staphylinid species (total S = 135) were caught exclusively in the Schwaebische Alb (10%, 20%). Concerning the community composition in regional distinct forest types, the carabid communities were significant different in beech and oak stands in the Schorfheide-Chorin region (5.2% of variation; Table 4). Other forest types did neither have an effect on carabid nor on staphylinid community composition.

3.4. The importance of forest type vs. environmental characteristics Several environmental variables strongly influenced beetle communities, but they did not completely cover the variance explained by forest types as shown in the ANOVA approach. Thus, all variables describing forest types remained in the simplified ANOVA (Table 3). The carabid abundance increased with the cover of the sub-canopy, while canopy cover and shrub cover negatively and richness of vascular plants positively influenced staphylinid abundance. Although the effect of shrub cover was not significant, it remained in the simplified model. Carabid richness increased with higher diversity of herbs and staphylinid richness was

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Fig. 3. Non-metric multidimensional scaling (NMDS), based on presence-absence of species using Bray–Curtis distance. For carabid and staphylinid beetles the centroid of each forest type in each region is shown. Error bars reflect standard deviations along NMDS1 and NMDS2.

positively influenced by diversity of the entire plant community, the cover of the sub-canopy and, marginally significant, by the amount of coarse woody debris. The ratio of forest-to-open habitat carabids decreased with increasing bare soils and increasing cover of herbs, while it was positively influenced by the number of tree stems. The ratio of staphylinids did not respond to environmental variables, indicating that forest and open habitat species are similarly affected by environmental variables. Variance partitioning revealed that the carabid and staphylinid community composition was mainly influenced by region followed by environmental variables and forest types. However, the jointly explained variances by region and environmental characteristics (both beetle families) and environment and forest types (Staphylinidae) was higher than of their components alone (Fig. 4).

should be handled with care and that differing forestry practices among regions as well as geographic variation of beetle communities might cause different responses to forestry management. Although inter-regional effect of forest types was low in our study we observed some general effects on the focal taxa, namely there were fewer individuals in young stands than in older ones and higher species richness in managed stands than in unmanaged forests. Below, we discuss the factors that may have contributed to the general as well as regional specific effects and how these findings might help to improve forest management and conservation strategies.

4. Discussion

Despite the strong variability of the beetle community structure among regions, we could show clear general effects of forest types on both families of ground-dwelling beetles; beetles were generally (1) more rich in managed than in recently unmanaged stands and (2) less abundant in younger stands than in older ones. This finding is in contrast to the meta-analysis of Paillet et al. (2010), who compared unmanaged and managed forests across Europe and reported negative effects of forest management on species richness of various taxonomic groups, including carabids. However, a main drawback of this meta-analysis is that three-quarters of the considered studies dealing with carabids were conducted in boreal forests – the limitations of which were highlighted by Halme et al. (2010). The different findings might therefore indicate

Our inter-regional study revealed that forest management in Central Europe has multifaceted effects on ground-dwelling beetles. The direction or strength of these effects varied strongly among regions and between carabids and staphylinids. This is in contrast to previous studies focusing on a particular region. They found more clear-cut results, mainly decreasing arthropod diversity with increasing management and proposed general conclusions for conservation oriented forest management from these observations (e.g. Niemelä et al., 1996; Magura et al., 2002; de Warnaffe and Lebrun, 2004; Fuller et al., 2008). Our findings indicate that generalization of results obtained in a single region

4.1. Influence of forest types on beetle community structure and composition

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(a)

(b)

Carabidae Region

0.09

Forest type

0.02

0.04

Staphylinidae Region

0.10

0.00

0.02

0.01

0.06 0.12

Forest type

0.11

0.08

0.18

0.07

0.06

Environment

Environment Residuals = 0.51

Residuals = 0.54

Fig. 4. Variance partitioning of the community compositions (relative abundances) of carabid and staphylinid beetles. The explained and shared variance of region, forest types and environmental characteristics (Table A.2) are shown.

that effects of forestry differ among different climatic zones (e.g. Lange et al., 2011b). In line with our results, de Warnaffe and Lebrun (2004) observed a lower species richness of carabids in unmanaged Belgian beech forests than in managed beech stands. The authors attributed their findings to the relatively short time since abandonment (100 years) and to the very slow re-colonization ability of forest specialists, once they went locally extinct. The stands in our study were abandoned for an even shorter period of time (between 20 and 70 years), which might explain the low overall richness in these forest stands. We did not observe lower richness of forest species, but a higher richness of open habitat species in managed stands. Thus, the higher overall richness of carabids and staphylinids in managed forest stands is due to additional open habitat species with suggested fast colonization ability (Niemelä et al., 2007). This is also supported by the higher abundance ratio of carabid forest-to-open habitat species (staphylinids) in unmanaged forests of our study. Thus, focusing on species composition regarding ecological (e.g. habitat preference as performed in present study) or morphological traits (e.g. dispersal ability) rather than species richness might be more suitable to characterize the conservation value of a forest than species numbers or diversity per se (Niemelä, 1997). Furthermore, the lower number of carabids and staphylinids in younger stands indicates either reduced resource availability in the young stands or an early colonization stage of the beetle community in young forest stands. Community composition of carabids and staphylinid responded similarly to recent forestry history and stand age by showing significant differences between managed and unmanaged as well as between young and old stands. However, the greatest difference in the composition of both focal taxa was between coniferous and beech stands, and this was particularly pronounced in staphylinids. This points to the large impact of tree plantations, non-natural to the site, on invertebrate communities (Elek et al., 2001). This indicates preference for forest stands of particular natural tree species in generalist predatory beetles and this might be mainly due to differences in soil moisture (Sroka and Finch, 2006; Worthen and Merriman, 2013). The described patterns of community structure were not driven by the most abundant beetle species (Table A.7), as the effect of forest types remained consistent when dominant beetle species were excluded (Table A.8). Not surprisingly, however, the influence of forest types on species composition was highly affected by the dominating species in both, carabid and staphylinid beetles (Table A.9).

4.2. Relative importance of environmental characteristics and forest types to beetle communities We found single environmental variables to be highly important in driving beetle community structures (abundance, species richness and ratio of forest-to-open habitat species). These were in particular canopy cover for carabid abundance and different plant diversity means for staphylinid abundance and for the richness of both focal taxa. Disturbances to canopy cover generally increase plant species richness in forest stands investigated in this study (Boch et al., 2013). Thus both, the more open forest structure and the more divers vegetation on the forest floor might favor immigration of additional species, which are more associated with open habitats. Unexpectedly, the environmental variables did not mediate the effect of forest types completely. This suggests that some changes might be mediated by non-measured variables such as soil moisture. Surprisingly within managed forest the community structure of beetles in uneven-aged (selection-cutting) and mixed (beech-pine) forest stands did not differ from even-aged forest stands. These forestry methods are expected to promote a higher structural heterogeneity in the canopy with a more complex spatial canopy gap distribution than even-aged management (Getzin et al., 2011; Wagner et al., 2011) and a higher vertical structuring. As higher structural heterogeneity should translate into higher niche diversity and thus higher resource availability for predators, according to the ‘Enemies hypothesis’, we would have expected a higher abundance and richness of ground-dwelling carabids and staphylinids in these forest types. However, this was not the case. Our findings are in line with the results of de Warnaffe and Lebrun (2004), who found a low impact of local canopy heterogeneity on richness of carabids when comparing even-aged to uneven-aged stands. Furthermore, recent findings of Barsoum et al. (2014)) and Oxbrough et al. (2012) who showed that species richness and assemblage structure of carabid beetles did not differ between monoculture and mixed species stands in Ireland, are in line with our results. 4.3. Geographic inconsistencies The results regarding community structure as well as community composition showed inter-regional variations. The observed significant interactions between region and forest types in the ANOVAs were further supported by the high values of shared variance by two groups of variables in the variance partitioning

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approach (Fig. 4). In particular the abundance of both, carabid and staphylinid beetles differed in their response to the dominant tree species among regions, being prevalent only in the SchorfheideChorin. Microclimatic conditions differ highly between beech/ spruce and pine forests with latter being more open and dry. Thus the great differences in humidity and soil moisture between beech and pine forests might explain the observed community response to the dominant tree species in this region. Regarding species richness only staphylinid beetles differed in their response to recent forestry history and dominant tree species among regions. These inconsistent responses might be caused by geographic variation in species pools which might be a consequence of historic forest management and/or changes in habitat preferences among regions (see also Gossner et al., 2014). In carabids the forest-to-open habitat species ratio showed inconsistencies in its response to recent forestry history and dominating tree species among regions. The higher proportion of open-habitat species in conifer plantations in the SchorfheideChorin can be explained by the more open pine forests compared to the spruce forests occurring in the Schwaebische Alb and the Hainich-Duen. To reveal the underlying mechanisms of the observed pattern that the proportion of forest species is higher in unmanaged compared to managed forests in the Schwaebische Alb and the Schorfheide-Chorin, but opposite in the Hainich-Duen requires further investigations. 4.4. Differences between carabid and staphylinid beetles In general, forest type influenced both taxa in a similar way, i.e. the richness was lower in recently unmanaged forests than in managed stands and within managed stands the richness was higher in even-aged coniferous stands than in even-aged beech stands. The explained variance of species richness in both families was similar, but the staphylinid abundance was much more explained by forest types than carabid abundance. Thus, effects of management on carabid abundance might more strongly depend on other factors such as forest history on the longer term, which was not considered in our study (c.f. de Warnaffe and Lebrun, 2004). The flight ability of staphylinids, in contrast to carabids, which comprise a high percentage of non-flying species, might result in a higher mobility and thus in a higher dispersal rate. As Pohl et al. (2007) pointed out, staphylinids therefore have a greater tendency to escape from unsuitable conditions than carabid beetles. This might explain the higher management effects we observed for staphylinids compared to carabids. In turn, their ability to fly might enable staphylinid species that are associated with old-growth forests to a faster remigration after abandonment of forests where they once have vanished than carabid beetles. However, no general indicator species of both carabids and staphylinids were identified for unmanaged forests across regions, as reported in a recent study conducted in the same forests (Gossner et al., 2014). 4.5. Conclusions Our study across three regions in Germany suggests that the richness of habitat sensitive arthropods, such as ground-dwelling beetles, is not universally a good metric for the conservation value of Central European forests. Since almost all forests in temperate Europe have been managed in the past, most forests either lack typical structural attributes (e.g. high dead wood amount, structural diversity) and microclimatic conditions of old-growth forests today, or habitat continuity was interrupted. Thus, studied forest regions might be in general impoverished in indicator species for ancient forests which are sensible to forest management and might have low remigration potential. Most remaining forest species might be able to cope with current forest management practices

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and additionally habitat generalists and open habitat species might be favored by management. Thus, the abundance ratio of forest species-to-open habitat species seems to be a better descriptors of management intensity of Central European forests than the diversity of ground-dwelling beetles, at least for forests that have been historically intensively managed resulting in a lack of more sensitive species. Despite this consistent pattern, we observed several region-specific management effects on community structure and. Thus, to protect important forest beetle communities, possible geographic variations in the response of beetle communities need to be considered in conservation-orientated forest management strategies. Acknowledgments We thank the managers of the three Exploratories, S. Renner, S. Gockel, A. Hemp, M. Gorke and S. Pfeiffer for their work in maintaining the plot and project infrastructure, and late E. Kalko, K.E. Linsenmair, J. Nieschulze, F. Buscot, and E.-D. Schulze for their role in setting up the Biodiversity Exploratories Project. We are grateful to all colleagues and students who contributed to this study, to the local management teams for generous support of our study. Further, we thank B. Büche, M.-A. Fritze, T. Kölckebeck and F. Köhler for species identification and S.T. Meyer and J. Schumacher for fruitful discussion on statistical issues. Constructive comments of two anonymous reviewers improved the manuscript considerably. We are grateful to Shaun R. Levick for linguistic revision. The work has been funded by the DFG Priority Program 1374 ‘‘InfrastructureBiodiversity-Exploratories’’ (WE 3018/9-1). Field work permits were issued by the responsible state environmental offices of Baden-Wuerttemberg, Thuringia and Brandenburg (according to § 72 BbgNatSchG). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2014.06. 012. References Alalouni, U., Schaedler, M., Brandl, R., 2013. Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J. Appl. Entomol. 137, 721–738. Allegro, G., Sciaky, R., 2003. Assessing the potential role of ground beetles (Coleoptera, Carabidae) as bioindicators in poplar stands, with a newly proposed ecological index (FAI). For. Ecol. Manage. 175, 275–284. Ammer, U., Gossner, M., Gruppe, A., Simon, U., 2008. Integrating tree crown science with the development of ‘near-to-nature’ forest management practices: examples from Bavaria. In: Floren, A., (Ed.), Canopy Arthropod Research in Central Europe – Basic and Applied Studies from the High Frontier. Bioform Entomology, Nürnberg. Assmann, T., 1999. The ground beetle fauna of ancient and recent woodlands in the lowlands of north-west Germany (Coleoptera, Carabidae). Biodivers. Conserv. 8, 1499–1517. Baguette, M., 1993. Habiat selection of carabid beetle in deciduous woodlands of southern Belgium. Pedobiologia 37, 365–378. Barsoum, N., Fuller, L., Ashwood, F., Reed, K., Bonnet-Lebrun, A.-S., Leung, F., 2014. Ground-dwelling spider (Araneae) and carabid beetle (Coleoptera: Carabidae) community assemblages in mixed and monoculture stands of oak (Quercus robur L./Quercus petraea (Matt.) Liebl.) and Scots pine (Pinus sylvestris L.). For. Ecol. Manage. 321, 29–41. Bauhus, J., Puettmann, K., Messier, C., 2009. Silviculture for old-growth attributes. For. Ecol. Manage. 258, 525–537. Boch, S., Prati, D., Muller, J., Socher, S., Baumbach, H., Buscot, F., Gockel, S., Hemp, A., Hessenmoller, D., Kalko, E.K.V., Linsenmair, K.E., Pfeiffer, S., Pommer, U., Schoning, I., Schulze, E.D., Seilwinder, C., Weisser, W.W., Wells, K., Fischer, M., 2013. High plant species richness indicates management-related disturbances rather than the conservation status of forests. Basic Appl. Ecol. 14, 496–505. Böhme, J., 2005. Die Käfer Mitteleuropas. Bd. K-Katalog: Faunistische Übersicht. Elsevier GmbH, Spektrum Akademischer Verlag, Heroldsberg, Krefeld. Boncina, A., 2011. Conceptual approaches to integrate nature conservation into forest management: a Central European perspective. Int. Forest. Rev. 13, 13–22.

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