Most forests are exposed to anthropogenic management activities that affect tree species composition and natural ecosystem processes. Changes in ecosystem processes such as herbivory depend on management intensity, and on regional environmental conditions and species pools. Whereas influences of specific forest management measures have already been addressed for different herbivore taxa on a local scale, studies considering effects of different aspects of forest management across different regions are rare. We assessed the influence of tree species composition and intensity of harvesting activities on arthropod herbivores and herbivore-related damage to beech trees, Fagus sylvatica, in 48 forest plots in three regions of Germany. We found that herbivore abundance and damage to beech trees differed between regions and that – despite the regional differences - density of tree-associated arthropod taxa and herbivore damage were consistently affected by tree species composition and harvest intensity. Specifically, overall herbivore damage to beech trees increased with increasing dominance of beech trees – suggesting the action of associational resistance processes – and decreased with harvest intensity. The density of leaf chewers and mines was positively related to leaf damage, and several arthropod groups responded to beech dominance and harvest intensity. The distribution of damage patterns was consistent with a vertical shift of herbivores to higher crown layers during the season and with higher beech dominance. By linking quantitative data on arthropod herbivore abundance and herbivory with tree species composition and harvesting activity in a wide variety of beech forests, our study helps to better understand the influence of forest management on interactions between a naturally dominant deciduous forest tree and arthropod herbivores.
Citation: Mangels J, Blüthgen N, Frank K, Grassein F, Hilpert A, Mody K (2015) Tree Species Composition and Harvest Intensity Affect Herbivore Density and Leaf Damage on Beech, Fagus sylvatica, in Different Landscape Contexts. PLoS ONE 10(5): e0126140. https://doi.org/10.1371/journal.pone.0126140
Academic Editor: Martin Schädler, Helmholtz Centre for Environmental Research (UFZ), GERMANY
Received: November 25, 2014; Accepted: March 30, 2015; Published: May 4, 2015
Copyright: © 2015 Mangels et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: The work has been funded by the DFG Priority Program 1374 "Infrastructure-Biodiversity-Exploratories" (BL 960/2-1) to NB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Most forests have been considerably modified by human activities [1–3]. Anthropogenic influences affect forest ecosystems indirectly via activities including hunting, livestock grazing, environmental pollution, human-assisted biological invasions and climate change, but also directly via forest management activities [4–6]. Whereas it is evident that forest management such as logging and reforestation with mono- and polycultures of native or non-native tree species can affect forest biodiversity (sensu [7, 8]) and related ecosystem processes [9–11], the extent of these effects is more difficult to predict and supposedly contingent on the intensity of forest management and on the processes studied [12–15].
Herbivory, the consumption of plant material by animals, is a fundamental ecosystem process that affects nutrient cycles and plant abundance, and as a consequence resources and habitats for other organisms [16–18]. In forests, arthropod herbivores are abundant and diverse [19–21], and both abundance and diversity of herbivores are assumed to contribute to the extent of herbivory in forests [22–24], although the relationship between herbivore abundance, herbivore diversity and herbivory may also be ambiguous [25–27].
Herbivore diversity and abundance on host plants is modified by an array of different factors such as abiotic conditions [28, 29], the quality of host plants [30–32], and the exposure to competitors and natural enemies [33–35]. In forests, these factors may show strong vertical stratification within individual trees , and they may also be strongly influenced by tree species composition [37, 38]. Following the vertical stratification of resources and conditions within tree crowns, many arthropod herbivores show a stratified spatial distribution in the canopy [36, 39, 40]. Although a distinct stratification of arthropods has been described for both tropical and temperate forests, stratification seems to be no static characteristic of canopy arthropod assemblages, but it may vary between seasons and with tree species identity, tree age and tree neighborhood [36, 41, 42].
Tree neighborhood reflects age structure and species composition of neighbor trees and can thus be viewed as one aspect of the more general influence of forest management and tree species composition (tree association) on the abundance and diversity of herbivores on forest trees. Although plants in pure stands may often suffer from stronger herbivory than those in mixed stands, both positive and negative effects of plant association on herbivore damage have been reported [43–45]. Plant associations can increase or decrease herbivore density or herbivore damage and are referred to as "associational susceptibility" (AS) and "associational resistance" (AR) respectively . In forest systems, both AS and AR have been documented as a consequence of tree association, which is most commonly measured as tree diversity or dominance of a focal tree species [38, 46]. For example, insect herbivory on oaks and alders was lower in monocultures, whereas herbivory on birch was higher in pure birch stands . To explain such contrasting effects of plant association on plant damage, different hypotheses have been established. These hypotheses consider both bottom-up and top down processes (see [47, 48] for review of associational resistance hypotheses), and the influence of variation in species characteristics [45, 49].
Tree association in forests is strongly determined by forest management, which influences tree species composition and quality [50, 51], and thus directly and indirectly affects the abundance of herbivores [52, 53]. Besides determining tree association, forest management involves harvesting practices, which may, for example, change forest microclimate, host plant quality, host plant quantity, and enemy pressure [4, 54]. As a consequence of these changes in the abiotic and biotic environment, harvesting can have intensity-dependent effects on herbivores and on related damage to trees [55–57]. These effects may either decrease or increase herbivore populations and herbivore diversity depending on species characteristics such as dependence on specific hosts and successional stages of forest [58, 59]. In addition to the potentially strong influence of forest management on herbivore populations and herbivore diversity, all the effects should be regarded in the context of larger-scale environmental variation (including climate, edaphic conditions, landscape heterogeneity) and regional species pools. These factors can have a strong impact on herbivore abundance and damage, and they may dilute, overlay or interact with the effects of forest management [55, 60, 61].
Considering the varying and interacting effects of tree association, harvest intensity and regional environmental conditions on herbivores and their damaging activity, a simultaneous assessment of these factors appears necessary to achieve generalizable information on the major determinants of herbivory in forest ecosystems. In our study, we investigated herbivore density and damage to European beech trees (Fagus sylvatica L.) growing in forests with different management histories in three regions of Germany, to clarify the role of forest management on herbivore abundance and on related damage to trees across a variety of silvicultural and abiotic conditions. We focused on beech forests since European beech is the dominating tree species of the potential natural vegetation in Central Europe [62, 63]. Despite their dominant role in European forests, beech trees appear to suffer relatively low damage and to host a less speciose and abundant arthropod assemblage than other common deciduous trees such as oak and maple [64–66]. As increasing abundance and species-area relationships are generally related to increasing species richness [64, 67], the relatively low infestation and species richness of arthropod herbivores on beech emphasizes the need for investigations on determinants of herbivore-beech interactions.
Specifically, we investigated whether (1) herbivore abundance and damage vary between regions differing in various environmental conditions for the same forest type (beech forest) and whether (2) forest management, estimated by beech dominance and harvest intensity, affects herbivore abundance and damage under consideration of expected regional effects. In addition to regional patterns, we (3) also considered herbivore distribution and damage by specific arthropod taxa within tree crowns .
Material and Methods
Permits for field work were issued by the responsible state environmental offices of Brandenburg, Thüringen and Baden-Württemberg (according to § 72 BbgNatSchG). The study sites comprise state forests and protected areas such as the National Park Hainich and some nature reserves within the biosphere reserves Schwäbische Alb and Schorfheide-Chorin, as well as in the forest of Keula, Hainich-Dün. No species that are protected by European or national laws were sampled during this study.
The study was conducted in the framework of the German Biodiversity Exploratories Project (http://www.biodiversity-exploratories.de). The Biodiversity Exploratories Project addresses effects of land use on biodiversity and biodiversity-related ecosystem processes .
Leaf damage by herbivores was assessed in November 2012 (year 1) from fallen leaves and in May and July 2013 (year 2) from live leaves. The assessments in year 2 were also used to quantify herbivore load on study trees. Assessments were carried out in forest plots in the three Biodiversity Exploratories (from north to south) “Schorfheide-Chorin” (SCH; a glacial formed landscape in North-East Germany, 3–140 m a.s.l., 13°23’27”–14°08’53” E / 52°47’25”–53°13’26” N), “Hainich” (HAI; a hilly region in Central Germany, 285–550 m a.s.l., 10°10’24”–10°46’45” E / 50°56’14”–51°22’43” N), and “Schwäbische Alb” (ALB; a low-mountain range in South-West Germany, 460–860 m a.s.l., 09°10’49”–09°35’54” E / 48°20’28”–48°32’02” N). SCH is characterized by the lowest annual precipitation (520–580 mm), with a mean annual temperature of 6–7°C. It is followed by HAI (630–800 mm, 6.5–8°C) and ALB (800–930 mm, 8–8.5°C). More details on the Biodiversity Exploratories can be found in Fischer et al. (2010) .
In year 1, fallen leaves were collected on each corner of 15 plots in HAI and in ALB Exploratories. These plots included three different forest types (n = 5 plots per type and region): uncultivated, young and old beech forest. Leaf damage was then calculated as the percentage of leaf damage for 50 leaves randomly chosen per corner that were scanned and afterwards subjected to a pixel analysis using the software Image J . Percent leaf damage was calculated by estimating the number of pixels of the leaf area missing due to herbivory (attributable to chewing herbivores, not mines and galls) and by relating this number to the number of pixels of the whole leaf including intact and damaged leaf parts . In year 2, we collected live leaves of five beech trees randomly chosen in 16 plots per region. Additionally to beech forest, conifer forest (pines at SCH and spruces at HAI and ALB) was added in year 2 (n = 4 plots per Exploratory). For each selected beech tree, leaves of a lower and an upper position within the tree crown were considered, henceforth termed “crown position”. The leaves from heights below 2 meters were sampled with secateurs, whereas leaves from higher crown positions were sampled with a telescopic stick with a clipper at the end controlled by dint of a rope. To ensure that no arthropods escaped due to dropping during branch cutting, we collected those arthropods in a textile funnel positioned underneath the cut branch. The height of the sampled crown positions ranged between 10 cm and 10 m, and depended on the height of the sampled trees and on the accessibility of leaves by the ‘telescopic stick technique’ described above. The size of the sampled trees ranged from less than 1 meter high to fully-grown mature beeches. We estimated the height of the sampled tree (between 20 cm and 30 m) and counted the leaves of one branch per crown position (between 8 and 132 leaves, mean 36), estimated the percentage leaf damage attributable to chewing herbivores of each counted leaf with the aid of sample ‘leaf area loss’ cards (sensu ) (S1 Fig) and collected or registered all herbivores, galls and mines on the branch as a measure of herbivore load. In case that we encountered oaks (Quercus petraea Liebl. and Q. robur L.) or sycamore maples (Acer pseudoplatanus L.) in the plot, we analyzed herbivory and herbivores of three individuals of these tree species as well (and sampled only three beeches). We conducted the surveys in May when leaf-flushing in F. sylvatica starts, and during the midseason in July. We started each survey at SCH followed by HAI and ALB, an order that represented expression of tree phenology in the field (J. Mangels personal observation).
Mean values of leaf damage were calculated for each sampled tree per plot and per survey. Mean values were calculated in a similar way of the total number of herbivores, galls and mines per leaf for the surveys in year 2, as an estimator of herbivore density. We additionally calculated the coefficient of variation (CV) of herbivore damage across different trees within a plot, and compared damage patterns in different tree heights (two crown positions differing in height within a tree) based on a vertical stratification index VS = LDU/(LDU+LDL), where LDU is the leaf damage assessed at the upper crown position and LDL the damage at the lower position. For VS between 0 and 0.5, herbivore damage is higher in lower parts; values exceeding 0.5 indicate higher damage in the upper crown position. To compare leaf damage experienced by F. sylvatica with damage of other tree species, we conducted the same assessments of herbivore damage for individuals of Q. robur/petraea (n = 26) and A. pseudoplatanus (n = 70).
Forest management intensity
Defining forest management is a complex issue. The intensity usually varies gradually, which is not well mirrored in simple categorical classifications. To consider different aspects of forest management intensity, we used a combination of two predictor variables: (1) ‘beech dominance’ in the study plots, and (2) ‘harvest intensity’, measured as the proportion of harvested tree volume in the study plots (‘Iharv’: ). Beech dominance was assessed as the percentage of beech trees (in the shrub and the tree layer) among all tree individuals in the plot area ( and Fabrice Grassein, unpublished). The original forests in our study are dominated by beech—a higher proportion of beech trees thus assumedly reflects a lower management intensity. Beech dominance was also negatively related to tree diversity in the studied forest plots (beech dominance vs. Shannon diversity index: r = -0.416, p < 0.0001). Harvested tree volume in the study plots was quantified by Kahl and Bauhus as the ratio of harvested volume to the sum of standing, harvested and dead wood volume . In accordance with , we use the same term Iharv for harvested tree volume to address harvest intensity in our analyses.
Data were analyzed in generalized linear models (commands ‘glm’ for the model) using the statistical software package R 2.15.1 (R Core Team 2012) with the package ‘nlme’ . Leaf damage or herbivore densities were the response variables used in the model, with region (SCH, HAI and ALB), beech dominance and harvest intensity as the three fixed effect terms in a hierarchical order. The significance of the effect terms was tested using Chi2-tests (command “anova” based on sequential models of "type I"), and the differences between regions were assessed by Tukey post hoc tests following ANOVA. The data were transformed when necessary (see Table 1) to comply with the assumptions of variance homogeneity (Bartlett test) and normal distribution (Shapiro-Wilk test) of the residuals, and quasi-Poisson distribution was assumed when transformation was unsuccessful. In addition to the deviance and significance level of the GLM factors, we also show the linear regression coefficient for beech dominance and harvest intensity on response variables for a simple interpretation of response directions. To summarize impacts of forest management that may also appear via changes in beech dominance, an additional model for leaf damage was used where beech dominance was removed from the model. To elucidate the interaction effects between region and the continuous predictor variables beech dominance and harvest intensity, we additionally analyzed their effects on the response variables separately per region within the same generalized linear model. Finally, to compare leaf damage across different tree species, we used ANOVA (command ‘aov’) followed by Tukey post hoc tests.
Leaf damage by chewing herbivores differed considerably between regions (Fig 1, Table 1), and both the proportion of F. sylvatica (beech dominance) and harvest intensity affected the amount of leaf damage and the density of different taxonomic groups of herbivores when the regional differences were accounted for (Fig 2, Table 1). Damage of live leaves was highest in ALB (mean ± SD: 5.3 ± 2.9% in May and 8.1 ± 3.5% in July) and significantly lower in the two other regions (1.0–1.8 ± 0.4–1.9%) (Fig 1, Table 1). Similar results were observed for herbivore damage estimated on fallen leaves, with higher damage in ALB (3.2 ± 0.7%) than in HAI (1.3 ± 0.5%) (Fig 1c, Table 1).
Schorfheide (SCH), Hainich (HAI) and Schwäbische Alb (ALB)—in the surveys in May (a) and July 2013 (b) and November 2012 (c). The letters indicate significant differences between regions (ANOVA, Tukey’s post hoc p < 0.05).
Data were collected in May (a,b), July (c,d) and November (e,f) in the three regions Schorfheide (SCH), Hainich (HAI) and Schwäbische Alb (ALB).
Beech dominance showed a significant positive effect on leaf damage in May, with a significant effect in HAI, a marginally significant trend in ALB and a weak trend in SCH (Fig 2, Table 1, Supporting Information S1 Table). Even after accounting for region and beech dominance, harvest intensity had an additional effect on leaf damage in May, where leaf damage decreased significantly with increasing harvest intensity. The effect of harvesting in May remained significant when beech dominance was not considered as a predictor prior to harvesting in a sequential model (Table 1 footnote). The trends for leaf damage in July and for fallen leaves in November were similar, but not significant. Beech dominance and harvesting were not correlated (Pearson r = -0.19, p = 0.205).
Region and beech dominance significantly affected the vertical distribution of leaf damage (VS index) in May and July (Table 1). Herbivory was most pronounced in upper crown positions in May in ALB (mean VS ± SD: 0.61 ± 0.09), but in lower positions in HAI and SCH (0.44 ± 0.14 and 0.42 ± 0.12, respectively). VS values were significantly different from 0.5 (which would indicate a similar herbivory in lower and upper crown positions) in ALB (p = 0.04) and SCH (p = 0.006), but not in HAI (p > 0.05). Overall-VS values in May were not significantly different from 0.5. In July, the majority of herbivory was found in the upper crown positions (ALB: 0.56 ± 0.14, HAI: 0.57 ± 0.09, SCH: 0.48 ± 0.14), with overall-VS values and values from HAI being significantly higher than 0.5 (p = 0.04 and 0.003 for overall values and HAI, respectively). These results thus suggest an upward-shift of herbivore feeding in tree crowns during the season at least in HAI and SCH. In forests with high proportions of beech, herbivory was also more pronounced in higher crown positions (Table 1).
The variation of severity of herbivory across trees, expressed by the coefficient of variation (CV) of leaf damage, was not strongly differing between regions (Table 1). The only difference in CV was found between ALB and HAI for data on fallen leaves, where the CV of damage of fallen leaves was significantly lower in ALB (0.25 ± 0.09) than in HAI (0.38 ± 0.20). Beech dominance showed no effect on CV of leaf damage, whereas a weak negative effect (significant only in July) was detected for harvest intensity (Table 1).
Consistent with leaf damage, the abundance of all herbivore guilds—namely chewers, miners, aphids and galls—and of selected taxa, including weevils and lepidopteran caterpillars, significantly differed between regions (Table 1). Rhynchaenus (Orchestes) fagi L. was the most abundant weevil and represented 95% of all collected weevil individuals. As this species was detected exclusively in ALB, it was treated separately from the remaining weevils; region was removed as factor in the model. The results suggest that beech dominance and harvest intensity have no significant effect on R. fagi density. In contrast, beech dominance did have a significant negative effect on the density of aphids (represented by the woolly beech aphid Phyllaphis fagi L.) in both surveys, and a significant positive effect on mines and galls in May (Table 1). Harvest intensity had a positive effect on the density of weevils (excluding R. fagi) and on chewers in July (Table 1). Hence, contrasting responses to harvest intensity were found for leaf damage by chewing herbivores (negative in May) and these herbivore groups (positive) in different months.
A more detailed analysis on the family level of galling arthropods showed a positive effect of beech dominance on gall midges in May (r = 0.22; p = 0.005) and July (r = 0.32; p < 0.001) but no effect on gall mites. Analyses on the species level revealed that gall density of the gall mite Aceria nervisequa Cane. was positively related to beech dominance in May (r = 0.11, p = 0.027). Furthermore, beech dominance was positively related to gall density of the gall midges Mikiola fagi Hart. (May: r = 0.26, p = 0.016, July: r = 0.42, p < 0.001) and Phegomyia fagicola Kief. (July: r = 0.15, p < 0.001). Harvest intensity was positively related to gall density of the gall mite A. nervisequa in May (r = 0.28, p = 0.015) and to the gall midge P. fagicola in May (r = 0.25, p = 0.028).
Across all sites, average leaf damage and the total density of all leaf-chewing herbivores together were significantly positively correlated in May, but not July (Table 2). This was also confirmed for the caterpillars and for R. fagi alone, as well as for leaf mines that were not part of the damage assessment (Table 2).
Fagus sylvatica showed the lowest level of leaf damage compared to the other two studied tree species in July. Highest damage was found for Acer pseudoplatanus (mean ± SD: 8.7 ± 11.0), followed by Quercus spp. (4.2 ± 4.6%) and F. sylvatica (3.8 ± 5.2%). The factor tree species influenced leaf damage significantly (F = 14.27, p < 0.0001). The difference between damage of F. sylvatica and A. pseudoplatanus was highly significant (p < 0.0001). In May, where Quercus had not yet flushed leaves, A. pseudoplatanus (3.4 ± 6.4%) did not differ significantly from F. sylvatica (2.5 ± 3.8%).
In our study we investigated the effects of different aspects of forest management on the abundance of arthropod herbivores and on herbivore-related damage to beech trees, the prevailing tree species in natural Central European forests. Forest management was characterized by (1) changes in beech dominance, assuming that a low proportion of beech trees often represents targeted establishment of other timber species, and (2) by harvest intensity. Our results demonstrated that herbivore damage on beech trees may decline (depending on season) with decreasing beech dominance (i.e. a lower herbivory with increasing management intensity) and that it additionally may decline with increasing harvest intensity. The density of leaf chewers and mines was positively related to leaf damage, and several of the studied arthropod groups were found to respond to beech dominance and harvest intensity, albeit in different ways. An analysis of damage patterns in different tree heights indicated a vertical shift of herbivores to higher crown layers during the season and with higher beech dominance.
Regional differences in herbivore density and leaf damage
The regional differences found for herbivore density and leaf damage are in accordance with other studies showing strong differences in herbivore abundance and impact between study sites differing in climate and other environmental variables [42, 70, 74, 75]. Regional differences in abundance of insect species may be related to abiotic but also biotic environmental parameters, and they may occur for widespread as well as for site-restricted species (for a detailed discussion for German beech forests see [42, 76–78]). Whereas all groups of herbivores varied in abundance across regions in our study, this pattern was particularly obvious for abundance of the beech leaf-miner weevil R. fagi. This species can be considered as a key herbivore of beech [79–81], and it was the most numerous beetle species in our samples, but was only detected in one of the three regions (ALB). As R. fagi is known to occur throughout Germany , these marked differences in abundance are best explained by fluctuations in population density that are reportedly highly pronounced in this species (, and references therein). The importance of this species for herbivore damage in our study was supported by the high correlation of R. fagi density and overall leaf damage found in May, and the lower herbivore damage in HAI and SCH might be partially explained by the absence of this species.
Influence of forest management on leaf damage and herbivore density
Despite the strong regional differences in herbivore communities, consistent effects of tree species composition (beech dominance) and harvest intensity on herbivore density and damage were found. This finding emphasizes the potential importance of forest management for interactions between beech trees and their arthropod herbivores in different environmental contexts and it augments information obtained from qualitative herbivory assessments . The increase of damage to beech trees with beech dominance also suggests that some processes described by “associational resistance hypotheses” may hold for native Central European beech forests and are not restricted to agricultural [83, 84] or plantation [38, 45, 85] systems that are strongly influenced by land management. Associational resistance can be based on different processes, which may affect herbivores directly via plant traits such as suitability or apparency of focal plants (bottom-up processes), or via indirect effects on the herbivores’ enemies (top-down processes). Different bottom-up processes contribute to associational resistance (see [47, 48] for review of associational resistance hypotheses). As most of these hypotheses have been developed in short-lived agricultural systems—where initial host plant colonization is assumedly more important than in long-lived, perennial systems such as forests—or in young experimental forests, it is still a matter of ongoing investigations how they apply to mature or near-natural forest systems.
An increase of herbivory in pure stands is often explained by the resource concentration hypothesis [86, 87]. This hypothesis assumes that herbivores maintain higher densities and success in monospecific stands of their host plants, where presence of many conspecific plants enhances accessibility of host plants for specialist herbivores. In mixed stands, plant diversity may protect host plants by physically , visually [89, 90] or chemically [89–91] impeding herbivore access to the host plant. As herbivore species or even stages of the same herbivore species are strongly differing in their foraging behavior and responses to environmental parameters [92, 93], the specific mechanisms underlying an observed damage pattern can only be completely understood when the damaging species have been identified. In our study, this specific identification was obtained for a few species, namely the beech leaf-miner weevil R. fagi, the woolly beech aphid P. fagi and a few gall makers. The community of chewing herbivores as a whole responded in a positive way to beech dominance. However, the abundance of the only common chewing herbivore species that can be related to the quantified herbivore damage—the weevil R. fagi—did not respond to beech dominance in our analysis. The roles of other species need to be elucidated in more detailed studies in beech forests. Nevertheless, possible mechanisms can be deduced from other studies and systems. For example, positive relationships between herbivore damage and host plant dominance may occur in passively dispersing herbivores including early-instar moth larvae, where higher host density increases the probability to land on a suitable host, or for bark beetles, where higher host plant densities allow for buildup of critical population densities [92, 94, 95].
Increasing tree diversity (decreasing host dominance) may also increase herbivore damage, translating to associational susceptibility . This is particularly described for generalist herbivores profiting from mixing different host species, or spilling-over from preferred hosts to less palatable focal plants following exhaustion of the preferred host species [96, 97]. However, associational susceptibility due to increasing tree diversity is not restricted to generalist herbivores, but it can also occur for specialist herbivores avoiding enemies or competitors , or those that profit from mixing heterogeneous conspecific plants [98, 99]. In our study, an indication for associational susceptibility was found for infestation of beech by P. fagi, which was negatively related to beech dominance in spring and summer. In this case, a higher dominance of host trees may dilute the density of early-season fundatrices , or it may affect the quality of beech trees as a host. Host quality of trees may depend on tree association, for example as a consequence of facilitation and reduced stress in mixed stands during periods of abiotic stress such as drought , which is known to affect the suitability of trees for insect herbivores [102–104], depending on drought intensity[105, 106].
The change in associational effects—from support to suppression of herbivores—by increasing tree diversity (decreasing beech dominance) may also be related to indirect effects of enemies as stated by the enemies hypothesis [86, 107]. It is generally assumed that natural enemies of herbivores may profit from increasing plant diversity due to an increasing availability of resource and habitat conditions . In forests, these positive effects of increasing tree diversity have been shown for some predator or parasitoid groups but not for others [38, 65, 108, 109]. To assess whether top-down processes have contributed to effects of beech dominance on herbivores in our study, further investigations on enemy assemblages and on specific herbivores are required.
Besides effects of beech dominance, we also detected an influence of harvest intensity—defined as the proportion of harvested tree volume—on leaf damage and on abundance of some chewing herbivores. Harvesting activities may lead to a simplification of forest structure, which may provoke a reduction of herbivore abundance or species richness [110–112] in different taxonomic groups [14, 113]. These reductions in herbivore occurrence (including both abundance and diversity) may lead to a decrease in leaf consumption, which might explain the observed negative relationship between harvest intensity and herbivore damage in spring and also autumn (see also , who found a negative relationship between land use intensity and herbivory in grasslands). The decrease in herbivory might also come along with increased enemy pressure in more strongly disturbed forests, which might be possible for some key enemies [115–117], but is not generally to be expected ( and references therein).
Relationship between herbivore density and damage
We found a generally positive relationship between herbivore density and damage although such a pattern may not always be apparent given the conceptual differences between the two parameters: whereas the assessment of damage integrates over a period of time, the activities of specific herbivores are usually fluctuating over the season and with changes in environmental conditions or resource availability . In our study this shift became apparent by the observed switch of herbivory from lower to higher canopy layers. These shifts may directly track resource availability and quality, but they may also reflect changes in species composition . The shifts in resources and species may also explain why we did not detect effects of beech dominance and harvest intensity on damage later in the season—probably since different effects were masking each other.
Our study showed that the occurrence of arthropod herbivores in forests and resulting damage to forest trees is influenced by host tree dominance and by differences in harvest intensity. Specifically, herbivore damage to beech trees increased with increasing dominance of beech trees and decreased with increasing harvest intensity. These findings appear to be generalizable at least for European beech forests as they were consistent across forests from three regions varying in biotic and abiotic environmental conditions. At the same time, strong temporal and spatial variation in herbivore occurrence and damage to beech, but also to oak and maple trees, point to the highly conditional nature of herbivory as an ecosystem process.
S1 Fig. Calculated percentage damage of a fictive beech leaf to support the estimation of damage of sampled leaves.
S1 Table. Complementary analysis (see Table 1) of significant interaction effects between region, beech dominance and harvest intensity.
We thank Roswitha Ehnes for help with leaf collection, Tiemo Kahl for providing data on harvest intensity in the studied plots, and the managers of the three Exploratories, Swen Renner, Sonja Gockel, Kerstin Wiesner, and Martin Gorke for their work in maintaining the plot and project infrastructure; Simone Pfeiffer and Christiane Fischer giving support through the central office, Michael Owonibi for managing the central data base, and Markus Fischer, Eduard Linsenmair, Dominik Hessenmöller, Jens Nieschulze, Daniel Prati, Ingo Schöning, François Buscot, Ernst-Detlef Schulze, Wolfgang W. Weisser and the late Elisabeth Kalko for their role in setting up the Biodiversity Exploratories project. The work has been funded by the DFG Priority Program 1374 "Infrastructure-Biodiversity-Exploratories" (BL 960/2-1). Field work permits were issued by the responsible state environmental offices of Baden-Württemberg, Thüringen, and Brandenburg (according to § 72 BbgNatSchG).
Conceived and designed the experiments: NB KM JM. Performed the experiments: JM KF AH FG. Analyzed the data: JM NB KM. Wrote the paper: JM KM NB FG.
- 1. FAO (2010) Global forest resources assessment 2010. Main report. Rome: Food and Agriculture Organization of the United Nations.
- 2. Paquette A, Messier C (2010) The role of plantations in managing the world's forests in the Anthropocene. Front Ecol Environ 8: 27–34.
- 3. Powers RF (1999) On the sustainable productivity of planted forests. New Forest 17: 263–306.
- 4. Jactel H, Nicoll BC, Branco M, Ramon Gonzalez-Olabarria J, Grodzki W, Langstrom B, et al. (2009) The influences of forest stand management on biotic and abiotic risks of damage. Ann For Sci 66. pmid:21423861
- 5. Milad M, Schaich H, Burgi M, Konold W (2011) Climate change and nature conservation in Central European forests: a review of consequences, concepts and challenges. For Ecol Manage 261: 829–843.
- 6. Pautasso M, Dehnen-Schmutz K, Holdenrieder O, Pietravalle S, Salama N, Jeger MJ, et al. (2010) Plant health and global change—some implications for landscape management. Biol Rev 85: 729–755. pmid:20105153
- 7. Fischer M, Bossdorf O, Gockel S, Hänsel F, Hemp A, Hessenmöller D, et al. (2010) Implementing large-scale and long-term functional biodiversity research: the Biodiversity Exploratories. Basic Appl Ecol 11: 473–485.
- 8. Wilson EO (1992) The Diversity of Life. Cambridge, MA: Harvard University Press.
- 9. Gamfeldt L, Snall T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, et al. (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nature Commun 4.
- 10. Hunter ML (1999) Maintaining Biodiversity in Forest Ecosystems. Cambridge University Press. 720 p.
- 11. Petersen C, Woods HA, Kingsolver JG (2000) Stage-specific effects of temperature and dietary protein on growth and survival of Manduca sexta caterpillars. Physiol Entomol 25: 35–40.
- 12. Levers C, Verkerk PJ, Müller D, Verburg PH, Butsic V, Leitão PJ, et al. (2014) Drivers of forest harvesting intensity patterns in Europe. For Ecol Manage 315: 160–172.
- 13. Schall P, Ammer C (2013) How to quantify forest management intensity in Central European forests. Eur J For Res 132: 379–396.
- 14. Paillet Y, Berges L, Hjalten J, Odor P, Avon C, Bernhardt-Romermann M, et al. (2010) Biodiversity differences between managed and unmanaged forests: meta-analysis of species richness in Europe. Conserv Biol 24: 101–112. pmid:20121845
- 15. Riedel J, Dorn S, Plath M, Potvin C, Mody K (2013) Time matters: temporally changing effects of planting schemes and insecticide treatment on native timber tree performance on former pasture. For Ecol Manage 297: 49–56.
- 16. Boyd IL, Freer-Smith PH, Gilligan CA, Godfray HCJ (2013) The consequence of tree pests and diseases for ecosystem services. Science 342: 1235773. pmid:24233727
- 17. Metcalfe DB, Asner GP, Martin RE, Espejo JES, Huasco WH, Amezquita FFF, et al. (2014) Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol Lett 17: 324–332. pmid:24372865
- 18. Schowalter TD (2006) Herbivory. In: Schowalter T. D., editor editors. Insect ecology: an ecosystem approach. Amsterdam: Elsevier Academic Press. pp. 347–382.
- 19. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27: 305–335.
- 20. Elderd BD, Rehill BJ, Haynes KJ, Dwyer G (2013) Induced plant defenses, host-pathogen interactions, and forest insect outbreaks. Proc Natl Acad Sci USA 110: 14978–14983. pmid:23966566
- 21. Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Evol S 36: 597–620.
- 22. Vehviläinen H, Koricheva J, Ruohomäki K (2007) Tree species diversity influences herbivore abundance and damage: meta-analysis of long-term forest experiments. Oecologia 152: 287–298. pmid:17356813
- 23. Salazar D, Marquis RJ (2012) Herbivore pressure increases toward the equator. Proc Natl Acad Sci USA 109: 12616–12620. pmid:22802664
- 24. Schowalter TD, Lowman MD (1999) Forest herbivory: insects. In: Walker E. D., editor editors. Ecosystems of disturbed ground. Amsterdam: Elsevier. pp. 253–269.
- 25. Hartley MK, Rogers WE, Siemann E (2010) Comparisons of arthropod assemblages on an invasive and native trees: abundance, diversity and damage. Arthropod Plant Interact 4: 237–245.
- 26. Nummelin M (1992) Invertebrate herbivory in the forest floor vegetation of virgin and managed forest sites in the Kibale Forest, western Uganda. Afr J Ecol 30: 213–222.
- 27. Peter F, Berens DG, Farwig N (2014) Effects of local tree diversity on herbivore communities diminish with increasing forest fragmentation on the landscape scale. PloS one 9.
- 28. Schowalter TD (2012) Insect responses to major landscape-level disturbance. Annu Rev Entomol 57: 1–20. pmid:21888518
- 29. Seidl R, Fernandes PM, Fonseca TF, Gillet F, Jonsson AM, Merganicova K, et al. (2011) Modelling natural disturbances in forest ecosystems: a review. Ecol Model 222: 903–924.
- 30. Cornelissen T, Wilson Fernandes G, Vasconcellos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117: 1121–1130.
- 31. Lavandero B, Labra A, Ramírez CC, Niemeyer HM, Fuentes-Contreras E (2009) Species richness of herbivorous insects on Nothofagus trees in South America and New Zealand: the importance of chemical attributes of the host. Basic Appl Ecol 10: 10–18.
- 32. Poelman EH, Dam NM, Loon JJA, Vet LEM, Dicke M (2009) Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90: 1863–1877. pmid:19694135
- 33. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10: 977–994. pmid:17855811
- 34. Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40: 573–592.
- 35. Schmitz OJ, Barton BT (2014) Climate change effects on behavioral and physiological ecology of predator-prey interactions: implications for conservation biological control. Biol Control 75: 87–96.
- 36. Ulyshen MD (2011) Arthropod vertical stratification in temperate deciduous forests: implications for conservation-oriented management. For Ecol Manage 261: 1479–1489.
- 37. Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Syst 40: 1–20.
- 38. Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10: 835–848. pmid:17663717
- 39. Leksono AS, Nakagoshi N, Takada K, Nakamura K (2005) Vertical and seasonal variation in the abundance and the species richness of Attelabidae and Cantharidae (Coleoptera) in a suburban mixed forest. Entomolog Sci 8: 235–243.
- 40. Su JC, Woods SA (2001) Importance of sampling along a vertical gradient to compare the insect fauna in managed forests. Environ Entomol 30: 400–408.
- 41. Didham RK, Springate ND (2003) Determinants of temporal variation in community structure. In: Basset Y., Novotny V., Miller S. E. and Kitching R. L., editors. Arthropods of Tropical Forests: Spatio-temporal Dynamics and Resource Use in the Canopy. Cambridge: Cambridge University Press. pp. 28–39.
- 42. Gossner MM, Pasalic E, Lange M, Lange P, Boch S, Hessenmöller D, et al. (2014) Differential responses of herbivores and herbivory to management in temperate European beech. PloS one 9: e104876. pmid:25119984
- 43. Agrawal AA, Lau JA, Hamback PA (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Q Rev Biol 81: 349–376. pmid:17240728
- 44. Heiermann J, Schütz S (2008) The effect of the tree species ratio of European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst.) on polyphagous and monophagous pest species—Lymantria monacha L. and Calliteara pudibunda L. (Lepidoptera: Lymantriidae) as an example. For Ecol Manage 255: 1161–1166.
- 45. Plath M, Dorn S, Riedel J, Barrios H, Mody K (2012) Associational resistance and associational susceptibility: specialist herbivores show contrasting responses to tree stand diversification. Oecologia 169: 477–487. pmid:22159991
- 46. Koricheva J, Vehvilainen H, Riihimaki J, Ruohomaki K, Kaitaniemi P, Ranta H (2006) Diversification of tree stands as a means to manage pests and diseases in boreal forests: myth or reality? Can J Forest Res 36: 324–336.
- 47. Jactel H, Brockerhoff E, Duelli P (2005) A test of the biodiversity—stability theory: meta-analysis of tree species diversity effects on insect pest infestations, and re-examination of responsible factors. In: Scherer-Lorenzen M., Körner C. and Schulze E.-D., editors. Forest Diversity and Function: Temperate and Boreal Systems. Berlin, Heidelberg: Springer-Verlag. pp. 236–262.
- 48. Poveda K, Gomez MI, Martinez E (2008) Diversification practices: their effect on pest regulation and production. Rev Colomb Entomol 34: 131–144.
- 49. Castagneyrol B, Jactel H, Vacher C, Brockerhoff EG, Koricheva J (2014) Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J Appl Ecol 51: 134–141.
- 50. Hermy M, Verheyen K (2007) Legacies of the past in the present-day forest biodiversity: a review of past land-use effects on forest plant species composition and diversity. Ecol Res 22: 361–371.
- 51. Forkner RE, Marquis RJ (2004) Uneven-aged and even-aged logging alter foliar phenolics of oak trees remaining in forested habitat matrix. For Ecol Manage 199: 21–37.
- 52. Savilaakso S, Koivisto J, Veteli TO, Pusenius J, Roininen H (2009) Long lasting impact of forest harvesting on the diversity of herbivorous insects. Biodivers Conserv 18: 3931–3948.
- 53. Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31: 177–196.
- 54. Forkner RE, Marquis RJ, Lill JT, Le Corff J (2006) Impacts of alternative timber harvest practices on leaf-chewing herbivores of oak. 20: 429–440. pmid:16903104
- 55. Schowalter TD (1995) Canopy arthropod communities in relation to forest age and alternative harvest practices in western Oregon. For Ecol Manage 78: 115–125.
- 56. Summerville KS (2011) Managing the forest for more than the trees: effects of experimental timber harvest on forest Lepidoptera. Ecol Appl 21: 806–816. pmid:21639046
- 57. Watt AD (1992) Insect pest population dynamics: effects of tree species diversity. In: Cannell M. G. R., Malcolm D. C., Robertson P. A., editors. The Ecology of Mixed-Species Stands of Trees. Oxford. pp. 267–275.
- 58. Paquette A, Bouchard A, Cogliastro A (2006) Survival and growth of under-planted trees: a meta-analysis across four biomes. 16: 1575–1589. pmid:16937819
- 59. Rosenvald R, Lohmus A (2008) For what, when, and where is green-tree retention better than clear-cutting? A review of the biodiversity aspects. 255: 1–15.
- 60. Franklin AJ, Liebhold AM, Murray K, Donahue C (2003) Canopy herbivore community structure: large-scale geographical variation and relation to forest composition. Ecol Entomol 28: 278–290.
- 61. Summerville KS and Crist TO (2008) Structure and conservation of lepidopteran communities in managed forests of northeastern North America: a review. Can Entomol 140: 475–494.
- 62. Ellenberg H, Leuschner C (2010) Vegetation Mitteleuropas mit den Alpen. Stuttgart: Ulmer. XXIV + 1334 p.
- 63. Packham JR, Thomas PA, Atkinson MD, Degen T (2012) Biological flora of the British isles: Fagus sylvatica. J Ecol 100: 1557–1608.
- 64. Brändle M, Brandl R (2001) Species richness of insects and mites on trees: expanding Southwood. J Anim Ecol 70: 491–504.
- 65. Sobek S, Scherber C, Steffan-Dewenter I, Tscharntke T (2009) Sapling herbivory, invertebrate herbivores and predators across a natural tree diversity gradient in Germany’s largest connected deciduous forest. Oecologia 160: 279–288. pmid:19238448
- 66. Yela JL, Lawton JH (1997) Insect herbivore loads on native and introduced plants: a preliminary study. Entomol Exp Appl 85: 275–279.
- 67. Kennedy CEJ, Southwood TRE (1984) The number of species of insects associated with British trees: a re-analysis. J Anim Ecol 53: 455–478.
- 68. Rasband W (1997) ImageJ 1.46r. National Institutes of Health, USA.
- 69. Mody K and Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29: 217–225.
- 70. Adams JM, Fang W, Callaway RM, Cipollini D, Newell E (2009) A cross-continental test of the Enemy Release Hypothesis: leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe. Biol Invasions 11: 1005–1016.
- 71. Kahl T, Bauhus J (2014) An index of forest management intensity based on assessment of harvested tree volume, tree species composition and dead wood origin. Nat conserv 7: 15–27.
- 72. Boch S, Prati D, Muller J, Socher S, Baumbach H, Buscot F, et al. (2013) High plant species richness indicates management-related disturbances rather than the conservation status of forests. Basic Appl Ecol 14: 496–505. pmid:23875758
- 73. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: Linear and Nonlinear Mixed Effects
- 74. Stoeckli S, Mody K, Gessler C, Patocchi A, Jermini M, Dorn S (2008) QTL analysis for aphid resistance and growth traits in apple. Tree Genet Genomes 4: 833–847.
- 75. Truxa C, Fiedler K (2012) Down in the flood? How moth communities are shaped in temperate floodplain forests. Insect Conserv Diver 5: 389–397.
- 76. Andersen AN (1997) Functional groups and patterns of organization in North American ant communities: a comparison with Australia. J Biogeogr 24: 433–460.
- 77. Connor EF, Courtney AC, Yoder JM (2000) Individuals-area relationships: the relationship between animal population density and area. Ecology 81: 734–748.
- 78. Gering JC, Crist TO, Veech JA (2003) Additive partitioning of species diversity across multiple spatial scales: implications for regional conservation of biodiversity. Conserv Biol 17: 488–499.
- 79. Nielsen BO (1978) Food resource partition in the beech leaf-feeding guild. Ecol Entomol 3: 193–201.
- 80. Phillipson J, Thompson DJ (1983) Phenology and intensity of phyllophage attack on Fagus sylvatica in Wytham Woods, Oxford. Ecol Entomol 8: 315–330.
- 81. Rheinheimer J, Hassler M (2010) Die Rüsselkäfer Baden-Württembergs. Heidelberg: Landesanstalt für Umwelt, Messungen und Naturschutz Baden-Württemberg; Verlag Regionalkultur.
- 82. Péré C, Bell R, Turlings TCJ, Kenis M (2011) Does the invasive horse-chestnut leaf mining moth, Cameraria ohridella, affect the native beech leaf mining weevil, Orchestes fagi, through apparent competition? 20: 3003–3016.
- 83. Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36: 561–586.
- 84. Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, et al. (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21: 9–21. pmid:21516884
- 85. Vehviläinen H, Koricheva J, Ruohomäki K, Johansson T, Valkonen S (2006) Effects of tree stand species composition on insect herbivory of silver birch in boreal forests. Basic Appl Ecol 7: 1–11.
- 86. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: fauna of collards (Brassica oleracea). Ecol Monogr 43: 95–120.
- 87. Vandermeer J (1989) The Ecology of Intercropping. Cambridge University Press. 237 p.
- 88. Perrin RM, Phillips ML (1978) Some effects of mixed cropping on the population dynamics of insect pests. Entomol Exp Appl 24: 385–393.
- 89. Castagneyrol B, Giffard B, Péré C, Jactel H (2013) Plant apparency, an overlooked driver of associational resistance to insect herbivory. J Ecol 101: 418–429.
- 90. Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on ‘appropriate/inappropriate landings’ by pest insects of cruciferous plants. Entomol Exp Appl 96: 91–102.
- 91. Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10: 321–346.
- 92. Hochuli DF (2001) Insect herbivory and ontogeny: how do growth and development influence feeding behaviour, morphology and host use? Austral Ecol 26: 563–570.
- 93. Moreau G, Eveleigh ES, Lucarotti CJ, Quiring DT (2006) Ecosystem alteration modifies the relative strengths of bottom-up and top-down forces in a herbivore population. J Anim Ecol 75: 853–861. pmid:17009749
- 94. Kemp WP, Simmons GA (1979) Influence of stand factors on survival of early instar spruce budworm. Environ Entomol 8: 993–996.
- 95. Speight MR, Wainhouse D (1989) Ecology and Management of Forest Insects. Oxford: Oxford Science Publication, Clarendon Press.
- 96. Brown BJ, Ewel JJ (1987) Herbivory in complex and simple tropical successional ecosystems. Ecology 68: 108–116.
- 97. White JA, Whitham TG (2000) Associational susceptibility of cottonwood to a box elder herbivore. Ecology 81: 1795–1803.
- 98. Castagneyrol B, Lagache L, Giffard B, Kremer A, Jactel H (2012) Genetic diversity increases insect herbivory on oak saplings. PloS one 7.
- 99. Mody K, Unsicker SB, Linsenmair KE (2007) Fitness related diet-mixing by intraspecific host-plant-switching of specialist insect herbivores. Ecology 88: 1012–1020. pmid:17536716
- 100. Kareiva P (1983) Influence of vegetation texture on herbivore populations: resource concentration and herbivore movement. In: Denno R. F. and McClure M. S., editors. Variable Plants and Herbivores in Natural and Managed Systems. New York: Academic Press. pp. 259–289.
- 101. Pretzsch H, Schutze G, Uhl E (2013) Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biol 15: 483–495. pmid:23062025
- 102. Gutbrodt B, Dorn S, Mody K (2012) Drought stress affects constitutive but not induced herbivore resistance in apple plants. Arthropod Plant Interact 6: 171–179.
- 103. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, et al. (2013) Drought predisposes pinon-juniper woodlands to insect attacks and mortality. New Phytol 198: 567–578. pmid:23421561
- 104. Jactel H, Petit J, Desprez-Loustau ML, Delzon S, Piou D, Battisti A, et al. (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Glob Change Biol 18: 267–276.
- 105. Banfield-Zanin JA, Leather SR (2015) Season and drought stress mediate growth and weight of the green spruce aphid on Sitka spruce. Agric For Entomol 17: 48–56.
- 106. Mody K, Eichenberger D, Dorn S (2009) Stress magnitude matters: different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecol Entomol 34: 133–143.
- 107. Riihimaki J, Kaitaniemi P, Koricheva J, Vehvilainen H (2005) Testing the enemies hypothesis in forest stands: the important role of tree species composition. Oecologia 142: 90–97. pmid:15322903
- 108. Nixon AE, Roland J (2012) Generalist predation on forest tent caterpillar varies with forest stand composition: an experimental study across multiple life stages. Ecol Entomol 37: 13–23.
- 109. Lange M, Türke M, Pašalić E, Boch S, Hessenmöller D, Müller J, et al. (2014) Effects of forest management on ground-dwelling beetles (Coleoptera; Carabidae, Staphylinidae) in Central Europe are mainly mediated by changes in forest structure. For Ecol Manage 329: 166–176.
- 110. Ayres MP, Lombardero MaJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262: 263–286. pmid:11087032
- 111. Bouget C, Lassauce A, Jonsell M (2012) Effects of fuelwood harvesting on biodiversity—a review focused on the situation in Europe. Can J For Res 42: 1421–1432.
- 112. Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu Rev Ecol Evol Syst 33: 1–23.
- 113. Dodd LE, Lacki MJ, Britzke ER, Buehler DA, Keyser PD, Larkin JL, et al. (2012) Forest structure affects trophic linkages: how silvicultural disturbance impacts bats and their insect prey. For Ecol Manage 267: 262–270.
- 114. Gossner MM, Weisser WW, Meyer ST (2014) Invertebrate herbivory decreases along a gradient of increasing land-use intensity in German grasslands. Basic Appl Ecol in press.
- 115. Gandhi KJK, Gilmore DW, Katovich SA, Mattson WJ, Zasada JC, Seybold SJ (2008) Catastrophic windstorm and fuel-reduction treatments alter ground beetle (Coleoptera: Carabidae) assemblages in a North American sub-boreal forest. For Ecol Manage 256: 1104–1123.
- 116. Way MJ (1977) Pest and disease status in mixed stands vs. monocultures: the relevance of ecosystem stability. In: Cherrett J. M. and Sagar G. R., editors. Origins of pest, parasite, disease and weed problems. Oxford: Blackwell Scientific Publications. pp. 127–138.
- 117. Sheehan W (1986) Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environ Entomol 15: 456–461.
- 118. Gaston KJ, McArdle BH (1994) The temporal variability of animal abundances: measures, methods and patterns. Philos T Roy Soc B 345: 335–358.
- 119. Ruhnke H, Schädler M, Klotz S, Matthies D, Brandl R (2009) Variability in leaf traits, insect herbivory and herbivore performance within and among individuals of four broad-leaved tree species. Basic Appl Ecol 10: 726–736.