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Relationships between Plant Diversity and the Abundance and α-Diversity of Predatory Ground Beetles (Coleoptera: Carabidae) in a Mature Asian Temperate Forest Ecosystem

Relationships between Plant Diversity and the Abundance and α-Diversity of Predatory Ground... A positive relationship between plant diversity and both abundance and diversity of predatory arthropods is postulated by the Enemies Hypothesis, a central ecological top-down control hypothesis. It has been supported by experimental studies and investigations of agricultural and grassland ecosystems, while evidence from more complex mature forest ecosystems is limited. Our study was conducted on Changbai Mountain in one of the last remaining large pristine temperate forest environments in China. We used predatory ground beetles (Coleoptera: Carabidae) as target taxon to establish the relationship between phytodiversity and their activity abundance and diversity. Results showed that elevation was the only variable included in both models predicting carabid activity abundance and a-diversity. Shrub diversity was negatively and herb diversity positively correlated with beetle abundance, while shrub diversity was positively correlated with beetle a- diversity. Within the different forest types, a negative relationship between plant diversity and carabid activity abundance was observed, which stands in direct contrast to the Enemies Hypothesis. Furthermore, plant species density did not predict carabid a-diversity. In addition, the density of herbs, which is commonly believed to influence carabid movement, had little impact on the beetle activity abundance recorded on Changbai Mountain. Our study indicates that in a relatively large and heterogeneous mature forest area, relationships between plant and carabid diversity are driven by variations in environmental factors linked with altitudinal change. In addition, traditional top-down control theories that are suitable in explaining diversity patterns in ecosystems of low diversity appear to play a much less pronounced role in highly complex forest ecosystems. Citation: Zou Y, Sang W, Bai F, Axmacher JC (2013) Relationships between Plant Diversity and the Abundance and a-Diversity of Predatory Ground Beetles (Coleoptera: Carabidae) in a Mature Asian Temperate Forest Ecosystem. PLoS ONE 8(12): e82792. doi:10.1371/journal.pone.0082792 Editor: Dafeng Hui, Tennessee State University, United States of America Received July 31, 2013; Accepted October 29, 2013; Published December 20, 2013 Copyright:  2013 Zou 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. Funding: This research was financially supported by the National Natural Science Foundation of China (31270478), the ‘111 Program’ of the Bureau of China Foreign Experts and the Ministry of Education (2008-B08044) and the Chinese Academy of Science and their Fellowship for International Scientists programme (2011T2S18). The funders 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. * E-mail: swg@ibcas.ac.cn (WS); jan.axmacher@web.de (JCA) resulting in predators catching and feeding on prey more Introduction effectively, so that a higher diversity in the plant community is Terrestrial arthropods play important roles in ecosystem believed to support a higher diversity and abundance also of functioning, for example in pollination, pest control and in predatory species [11,14]. occupying key positions in carbon and nutrient cycling through A positive association between phytodiversity and both diversity food-web links. These roles also strongly impact on plant diversity and abundance of herbivorous arthropods has been found in a patterns [1–4]. Simultaneously, plant species richness is also variety of ecological experiments [4,5,9,15], in low-diversity believed to affect diversity and abundance of arthropods grassland [16–18] and in agriculture fields [19,20]. Nonetheless, throughout the trophic chain via bottom-up effects [5]. An reports of negative relationships between plant diversity and the increase in plant diversity can generally enhance net primary diversity of arthropod taxa are also common, backed again with productivity [6,7], which in term provides more food resources for results from experiments [21], grassland ecosystems [22,23] and herbivorous arthropods, hence increasing the overall biomass of agricultural landscapes [24]. In complex forest ecosystems, a arthropod consumers [8,9]. Apart from this control via food number of studies report a positive feedback between the diversity source effects, arthropod consumers are also known to be of plants and herbivorous insects [25–27]. Other studies nonethe- influenced by top-down control via the abundance of their natural less also report a lack of significant relationships [28,29] or even enemies [10–12]. This control forms the basis of the ‘‘Enemies negative correlations [30,31]. Hypothesis’’ [13], which postulates that species-rich vegetation For studies investigating links between the phytodiversity and assemblages can provide more refuges and more stable prey the diversity and abundance of predatory arthropods, the Enemies availability for predators than plant species-poor assemblages, Hypothesis has been supported by a range of experimental studies PLOS ONE | www.plosone.org 1 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages [5,32–34] and by studies in agricultural [19,35] and grassland [36] [52] ). Of these, 31 plots were sampled both in 2011 and 2012. To ecosystems with relatively low phytodiversity levels. It is predicted increase sampling intensity in the birch forest where overall beetle that top-down control of herbivores by natural enemies would be abundance was very low, two additional birch forest plots were sampled in 2012. more predominant in a perennial ecosystem than annual ones due not least to the more consistent prey availability [21,37]. The associated positive link between plant diversity and the diversity Vegetation Survey and Carabids Sampling and abundance of predatory arthropods is therefore predicted to Each study plot had a size of 20620 m and divided equally be stronger in natural forest ecosystems in comparison to annual into four subplots. In the centre of each sub-plot, a pitfall trap was grassland and agriculture fields. Nonetheless, very little research placed. For the recording of the vegetation, the entire 400 m plot has been conducted to date into these links in the world’s was divided into 4 sub-plots, and all trees and shrubs were remaining mature forest ecosystems. The limited published data recorded in each of the resulting sub-plots. Herbaceous species suggests that areas of high phytodiversity do not automatically were recorded in four plots of 1 m that were randomly located support a high diversity in predatory arthropods [38]. The within each of the sub-plots. The number of individuals was underlying patterns are not yet well-understood, and more studies recorded for each plant species in each layer. The breast height into the links between the vegetation and predatory arthropod area was recorded for each tree specimen and the average height taxa in natural forest ecosystems are urgently needed [39,40]. was recorded for each shrub and herb species. Among important predatory arthropod taxa, ground beetles The pitfall traps for carabid sampling consisted of a 250 ml (Coleoptera: Carabidae) are one of the most species-rich families, plastic cup with an open diameter of 7.5 cm. To minimize the comprising more than 40,000 described species [41]. Members of attractant bias, we used saturated salt (NaCl) water as killing this family, which is chiefly composed of true predators and solution and to preserve specimens in the sampling period [53]. omnivorous species, have been widely used in ecological studies Each cup was filled to about half its volume with saturated salt due to their environmental sensitivity and the good knowledge water, with detergent added to break the water surface tension. base existing in relation to their taxonomy and ecology [41–46]. Above each trap, a solid aluminium roof of 10610 cm was placed Ground beetles are believed to generally benefit from high levels of to protect the solution from dilution and litter contamination. plant diversity [47], and their abundance and diversity is believed Carabids were continually sampled from early July to early August to directly impact on ecosystem functioning [41,48,49]. in 2011 and from late June to late August in 2012, with traps In our study, we used ground beetles as target group to analyse routinely emptied and refilled in about 10 day-intervals. As it was the relationship between abundance and diversity of predatory impossible to sample all plots on the same day due to the large arthropods and phytodiversity. The study was undertaken in one geographical area and other logistical reasons, sampling days of the largest remaining mature temperate forest ecosystems in varied between 22 and 34 for the different plots in 2011, and China. To our knowledge, this is the first study specifically between 42 and 65 days in 2012. focussing on diversity relationship between plants and predatory arthropods in species-rich, mature temperate forests in Asia. Our Data Analysis objectives were 1) to test if positive links between ground beetle Carabid activity abundance of each plot was calculated as the abundance and diversity and the diversity in plant species exist as overall number of sampled individuals divided by the total predicted by the Enemies Hypothesis, and 2) to establish how sampling period in days, resulting in a mean daily catching rate environmental factors affect the observed links. for each plot. Values were calculated for the entire sampling period in 2011 and 2012 to minimize effects of inter-annual Materials and Methods variations. Carabid a-diversity was measured as Fisher’s a,a widely used parametric index considered robust in measuring Ethics arthropod diversity of samples varying in sample size This study was carried out in Changbaishan Nature Reserve [28,31,54,55]. Shannon diversity of the vegetation was calculated and all samplings were permitted by the Changbaishan Nature individually for each plant layer based on the important value (IV) Reserve Management Center. The field study did not involve any of each plant species to avoid the bias from simple abundance- endangered or protected species. based calculations [56,57]. The IV contains three aspects reflecting the relative contributions of each plant species towards Study Area each layer: relative abundance (d), relative frequency (f) and th th Our study area is located on the northern slopes of Changbai relative dominance (h). The IV for i species in j sample plot is Mountain (E 127u439 –128u169;N 41u419 –42u519) in Jilin calculated as: Province, North-eastern China. The local climate is influenced by 0 1 summer monsoon rains. The study area experiences dry, windy spring conditions followed by a short, wet summer, a cool autumn B C 1 d h B i i C with widespread fog and a long, cold winter [50]. The pristine IV ~ z z , i,j B C S S S 3@P P P A forest vegetation is composed of evergreen and deciduous d = h i i coniferous and broad-leaved tree species. The forests on Changbai 1 1 1 Mountain follow a distinctive altitudinal zonation, with a mixed coniferous and broad-leaved forest zone below 1100 m, a mixed where d is the number of individuals, f is the number of subplots in coniferous forest zone between 1100 and 1500 m and a sub-alpine which the species occurred, n is the total number of subplots in a mixed coniferous forest zone between 1500 and 1800 m. The sample plot (4 in this case), and h is the breast height area for tree upper forest boundary is composed of birch forests reaching species and the height for shrub and herb species. elevations of up to 2100 m, followed by a tundra zone with Our modelling of plant-carabid relationships was based on dominating dwarf trees and shrub formations [51]. multiple linear regressions, where carabid activity abundance and We selected a total of 33 plots between altitudes of 700 m and a-diversity were used as response variables, respectively. A series of 2000 m, representing all aforementioned forest types (see details in stepwise linear regression analyses was performed to identify the PLOS ONE | www.plosone.org 2 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages most important independent variables. Stepwise selection was used plots represents the low elevation zone below 1000 m covered by with both forward selection for selection of variables contributing mixed coniferous and broad-leaved forests, while the second significantly (P = 0.05) towards the model and backward elimina- cluster consists of 9 plots located in a median elevation zone tion to verify that variables made no significant contribution in the between 1000 m and 1500 m, containing 3 plots within the mixed selection of new variables. Vegetation variables included the total coniferous and broad-leaved forest type and 6 plots within mixed number of plant species (PS), the Shannon diversity (H) for trees coniferous forests, and the cluster of the remaining 13 plots (TH), shrubs (SH) and herbs (HH), and the abundance density (D) represents the high elevation zone above 1500 m covered by sub- for trees (TD), shrubs (SD) and herbs (HD), respectively. alpine mixed coniferous forests and birch forests. Modelling included all vegetation parameters as independent Below 1000 m in the mixed coniferous and broad-leaved forest variables first and then added elevation as additional independent elevation zone, the first model using vegetation parameters as variable. independent variables indicated that carabid activity abundance To account for the substantial forest vegetation changes with was negatively associated with TH (b = 21.67, P = 0.002) (Table 2, changing elevation, we used Principal Components Analysis (PCA) Model 6, AIC = 5.37, adjusted R = 0.62, F = 17.37, P = 0.002), 2,8 based on the presence-absence data of plant species to establish the while the second model also included a positive relationship with existence of distinct sample clusters representing a relatively SD (b = 0.012, P = 0.012), with a highly significant overall model homogeneous vegetation composition and re-ran the linear fit (Table 2, Model 7, AIC = 21.79, adjusted R = 0.82, regression models separately for the different clusters. F = 23.07, P,0.001). At the intermediate elevation zone, only 2,8 All statistical analysis was carried out in R [58], using the TD (b = 0.002, P = 0.011) was included in predicting carabid packages ‘‘spaa’’ [59] to calculate the Shannon diversity index and activity abundance (Table 2, Model 8, AIC = 14.12, adjusted ‘‘Vegan’’ [60] to carry out the PCA and to calculate Fisher’s a R = 0.57, F = 11.65, P = 0.011). For the highest elevation zone, 1,7 values. SH (b =21.435, P,0.001) was the only independent variable included in the model (Table 2, Model 9, AIC = 21.13, adjusted Results R = 0.73, F = 32.65, P,0.001). 1,11 None of the vegetation diversity variables was significantly We recorded a total of 178 plant species belonging to 128 linked with carabid a-diversity in any of the three distinct elevation genera and 58 families. The tree layer was comprised of 32 species zones. Nonetheless, carabid a-diversity was linked to the belonging to 20 genera and 12 families; the shrub layer contained vegetation density parameters SD (b = 20.058, P = 0.021) at the 43 species of 28 genera and 15 families and the herb layer low elevation zone (Table 2, Model 10, AIC = 21.79, adjusted comprised 112 species representing 88 genera and 43 families. 2 R = 0.40, F = 7.74, P = 0.021) and TD (b = 20.004, P = 0.041) 1,11 Pitfall traps caught 4844 carabids. Ten specimens (0.2%) were not at the high elevation zone (Table 2, Model 11, AIC = 22.41, identified due to substantial damage. The remaining 4834 adjusted R = 0.27, F = 5.37, P = 0.041). Neither herb diversity 1,11 individuals were separated into 34 species and 13 morphospecies. nor herb density appears to be linked to either activity abundance A detailed species list has been provided in [52]. The overall or a-diversity of carabids at any of the three elevation zones. average daily activity abundance for the entire study area was 1.83 individuals per plot. Discussion Carabid-plant Relationships Firstly, our study underlines that changes in elevation were the Stepwise regression entering all vegetation parameters produced predominant drivers of changes in both, carabid abundance and a two subsequent models predicting carabid activity abundance. diversity patterns in CNR, while the overall phytodiversity was not The first model (adjusted R = 0.43, F = 24.63, P,0.001) 1,31 significantly correlated with either abundance or a-diversity of the included SH as significant negative (b =20.925, P,0.001) beetles. Parameters associated with altitudinal changes like predictor of carabid abundance, while the second model (adjusted temperature and precipitation are therefore more important in R = 0.51, F = 17.29, P,0.001) additionally included HH as 2,30 influencing the diversity of ground beetles than plant diversity per positively (b = 0.427, P = 0.02) affecting beetle abundance. The se, which is also consistent with findings for herbivorous insect Akaike information criterion (AIC) slightly decreased from 79.35 diversity patterns [28,29,61,62]. Accordingly, we believe that the to 75.34 (Table 1, Models 1 and 2). The model predicting carabid observed relationships between activity abundance and a-diversity a-diversity again included SH as main predictor (b = 0.571, of carabids and vegetation variables recorded for the entire P = 0.039), which in this case was positively correlated with elevational gradient are mainly driven by the underlying changes Fisher’s a values. Overall, this model performed not as well in the environmental factors. (Table 1, Model 4, adjusted R = 0.10, F = 4.65, AIC = 102.45). 1,31 Nonetheless, the observed, highly significant negative correla- When elevation was entered as additional independent variable, tion between carabid activity abundance and the diversity of MLR models for both, carabid activity abundance and a-diversity, shrubs stands in direct contradiction to the Enemies Hypothesis, only included this parameter as significant, with model fits which predicts a positive relationship with carabid abundance. markedly improved (AIC = 71.71, adjusted R = 0.54, Our observations also stand in contrast to most studies conducted F = 39.13, beta = 1.753, P,0.001, and AIC = 96.27, adjusted 1,31 in agricultural [19,35] and grassland ecosystems [36], which differ R = 0.26, F = 12.11, beta = 21.451, P = 0.002, respectively, 1,31 from our study site by their markedly lower overall phytodiversity. Table 1, Models 3 and 5). Models therefore predict an increased Similar to us, Koricheva et al. [63] also reported a negative beetle abundance at a reduced diversity with increasing elevation. relationship between plant diversity and activity abundance of predatory arthropods in a grassland ecosystem. One of the Carabid-plant Relationship in the Different Vegetation explanations they present for this negative trend was a reduction in Types predator activity density with an increase in herb density, but this The ordination plot of the first two principle components (PCs) trend was not supported by our investigations. However, our based on vegetation composition showed three distinctive clusters results are consistent with observations by Schuldt et al. [38] who along the elevational gradient (Figure 1). A first cluster of eleven observed that activity abundance of spiders was also reduced in PLOS ONE | www.plosone.org 3 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages Table 1. Stepwise linear regression models using activity abundance and Fisher’s a-diversity of carabids as dependent variables, respectively, only using vegetation parameters as independent variables (Model 1, 2 and 4) and including elevation as additional independent variable (Model 3 and 5). Selected Model Adjusted Model independent Std. Error Dependent variable No. R F P-value Model AIC variable(s) b of b t P-value Activity abundance 1 0.43 24.63 ,0.001 79.35 SH 20.925 0.186 24.96 ,0.001 2 0.51 17.29 ,0.001 75.34 SH 20.897 0.173 25.17 ,0.001 HH 0.427 0.174 2.45 0.02 3 0.54 39.13 ,0.001 71.71 ASL(km) 1.753 0.280 6.26 ,0.001 Fisher’s a-diversity 4 0.1 4.65 0.039 102.54 SH 0.571 0.265 2.16 0.039 5 0.26 12.11 0.002 96.27 ASL(km) 21.415 0.530 23.48 0.002 TH: Shannon diversity for trees; SH: Shannon diversity for shurbs: TD: the abundance density for trees; SD: the abundance density for shrubs; Low: low elevation zone of less than 1000 m; Middle: intermediate elevation zone of 1000–1500 m; High: high elevation zone of 1500–2000 m. doi:10.1371/journal.pone.0082792.t001 areas with an increased woody plant diversity in a natural forest in terrestrial ecosystems [68], traditional top-down control theories Zhejiang Province. Schuldt et al. [64] and Vehvila ¨ inen et al. [65] that are suitable in less heterogeneous ecosystems may overall be state that the abundance of predatory species depends more difficult to apply here [39]. strongly on the presence of specific tree species rather than on The reported positive relationship between carabid activity overall tree diversity. The lack of validity of the Enemies abundance and woody plant density at low and intermediate Hypothesis for complex forest ecosystems might therefore relate elevation zones potentially reflects a bottom-up effect: plots with a to the multifaceted interactions between specific plant species, high density in woody plants are likely to be very productive. High their herbivores and the predatory insect assemblages inhabiting woody plant density can not only enhance shading and soil these ecosystems [39,66]. Although we did not investigate the role moisture levels and hence create favourable microhabitats for of specific tree or shrub species and their functional groups, an carabids and their larvae [69], but also producing more leaf litter, increase in woody plant diversity can be linked to either, an which can in term improve soil fertility and increase food availability for carabids [70,71]. The negative correlations increase in their evenness or their species richness, and hence might potentially reflect a reduction in the overall dominance of between woody plant density and the a-diversity of carabids specific favourable species, which could explain the reduction in within low and high elevation forest communities might again relate to changes in arthropod diversity being related to changes in carabid abundance. Alternatively, a high plant diversity can potentially support a higher density of herbivorous arthropods in the woody plant species composition, rather than their overall natural forests [25–27,67], which might also result in a reduction diversity [23,72]. Additionally, impacts of plant diversity are known to decrease with increasing trophic levels [5,73], so that of predators’ overall foraging time and hence their recorded activity density [38]. An increased plant diversity and the impacts of the vegetation on the diversity of predatory insects is often quite complex. associated assumed increase in herbivores can furthermore The negative relationship between altitude and the a-diversity provide an increase in food sources and niches for competing predatory arthropod taxa such as spiders and ants, increasing the of carabids can be explained by the Harsh Environmental overall competition levels for prey and consequently reducing the Hypothesis. Accordingly, species at high altitudes experience overall abundance of carabids. As food chains and habitats are harsh climatic conditions requiring them to have broader overall much more complex in forests in comparison to most other tolerance ranges than species at low altitudes, which in term leads to wider distribution ranges with increasing elevation and to a higher species richness at low altitudes [74–76]. This hypothesis is supported by the observed increase in carabid species’ altitudinal ranges with increasing elevation that we previously reported [52]. A possible reason for the positive links between carabid activity abundance and elevation could be the reduction of competitors such as ants and other predatory arthropods [77] or changes in the activity patterns due to potential scarcity of food resources, which would also increase the number of specimens sampled at high altitudes. Our results finally showed that the density of herbaceous plants did not significantly influence carabid activity abundance nor their diversity, which stands in strong contrast to studies in grassland ecosystems that commonly record negative relationships [78–80]. Pitfall traps have been widely used in surveys of ground-dwelling Figure 1. PCA ordination plot based on vegetation composi- arthropods [42,78,81–84] and can be considered as a standard tion showing three distinct clusters (proportion variance method in ground beetle sampling [42]. Nonetheless, one of the explained for PC1 = 24% and for PC2 = 11%; eigenvalues for main known pitfalls of pitfall trapping is the dependency of the PC1 = 4.83 and PC2 = 2.12). doi:10.1371/journal.pone.0082792.g001 sampling rate on both the target population density and the PLOS ONE | www.plosone.org 4 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages Table 2. Results of stepwise linear regressions for the three elevational zones using activity abundance and Fisher’s a-diversity of carabids as dependent variables and vegetation parameters as independent variables. Selected Elevation Model Adjusted Model Model independent Std. Error Dependent variable zone No. R F P-value AIC variable(s) b of b tP-value Activity abundance Low 6 0.62 17.37 0.002 5.37 TH 21.670 0.401 24.17 0.002 7 0.82 23.07 ,0.001 21.79 TH 21.236 0.310 23.99 0.004 SD 0.012 0.004 3.24 0.012 Middle 8 0.57 11.65 0.011 14.12 TD 0.012 0.003 3.41 0.011 High 9 0.73 32.65 ,0.001 21.13 SH 21.435 0.251 25.71 ,0.001 Fisher’s a-diversity Low 10 0.40 7.74 0.021 21.79 SD 20.058 0.021 22.78 0.021 High 11 0.27 5.37 0.041 22.41 TD 20.004 0.157 22.32 0.041 TH: Shannon diversity for trees; SH: Shannon diversity for shurbs: TD: the abundance density for trees; SD: the abundance density for shrubs; Low: low elevation zone of less than 1000 m; Middle: intermediate elevation zone of 1000–1500 m; High: high elevation zone of 1500–2000 m. doi:10.1371/journal.pone.0082792.t002 individual specimen’s activity [78,85–87]. Factors affecting this China, such as Liangshui and Fenglin Natural Reserve in activity need to be taken into consideration when comparing pitfall Heilongjiang Province, are ideal study areas to substantiate results samples, and it has commonly been suggested that vegetation from species-rich temperate forests. These latter studies in some of density particularly of herbaceous species needs to be considered the last remaining highly diverse mature temperate forest in the respective data interpretation [79,80]. The negative impact ecosystems in NE China would also allow a better understanding of this density in grassland ecosystems is believed to be due to a of the complex inter-linkages between taxa and across trophic reduction in the ground beetle mobility caused directly by a dense levels, with particular foci on the role of the woody plant species herb layer [79,80]. However, our results strongly suggest that the composition on predator distribution patterns and on the density of this layer in the old-growth forests on Changbai mechanisms governing responses of herbivorous arthropods to Mountain is not dense enough to significantly affect carabids’ changes in plant diversity and species composition. movements, supporting the argument that the influence of the density in understory vegetation can be neglected when studying Acknowledgments forest carabid assemblages [38]. Nonetheless, controlled capture- We thank Professor Liang Hongbin and his group at the Institute of recapture experiments would be needed to evaluate the exact Zoology, Chinese Academy of Sciences for their great help with carabid effects which might be present. identification. We are also grateful for the kind support from the Overall, our results clearly indicate that, in highly complex Changbaishan Forest Ecosystem Research Station, the Changbaishan forest ecosystems, predatory arthropod abundance and diversity Nature Reserve Management Center, the Changbaishan Academy of patterns do not support traditional top-down control theories that Sciences and the Changbaishan Natural Museum. We also greatly appreciate the help with our fieldwork from Eleanor Warren-Thomas, are suitable for less complex ecosystems. To substantiate these Long Chao, Liu Min, Zhou Xiasai and Han Furen. conclusions and establish if the Enemies Hypothesis is generally unsuitable for complex forest ecosystem, we suggest long-term Author Contributions monitoring of a wider range of predatory arthropod groups (e.g. spiders, ants and centipedes) not only in temperate, but also in Conceived and designed the experiments: YZ WS FB JCA. 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PLOS ONE | www.plosone.org 7 December 2013 | Volume 8 | Issue 12 | e82792 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLoS ONE Pubmed Central

Relationships between Plant Diversity and the Abundance and α-Diversity of Predatory Ground Beetles (Coleoptera: Carabidae) in a Mature Asian Temperate Forest Ecosystem

PLoS ONE , Volume 8 (12) – Dec 20, 2013

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Abstract

A positive relationship between plant diversity and both abundance and diversity of predatory arthropods is postulated by the Enemies Hypothesis, a central ecological top-down control hypothesis. It has been supported by experimental studies and investigations of agricultural and grassland ecosystems, while evidence from more complex mature forest ecosystems is limited. Our study was conducted on Changbai Mountain in one of the last remaining large pristine temperate forest environments in China. We used predatory ground beetles (Coleoptera: Carabidae) as target taxon to establish the relationship between phytodiversity and their activity abundance and diversity. Results showed that elevation was the only variable included in both models predicting carabid activity abundance and a-diversity. Shrub diversity was negatively and herb diversity positively correlated with beetle abundance, while shrub diversity was positively correlated with beetle a- diversity. Within the different forest types, a negative relationship between plant diversity and carabid activity abundance was observed, which stands in direct contrast to the Enemies Hypothesis. Furthermore, plant species density did not predict carabid a-diversity. In addition, the density of herbs, which is commonly believed to influence carabid movement, had little impact on the beetle activity abundance recorded on Changbai Mountain. Our study indicates that in a relatively large and heterogeneous mature forest area, relationships between plant and carabid diversity are driven by variations in environmental factors linked with altitudinal change. In addition, traditional top-down control theories that are suitable in explaining diversity patterns in ecosystems of low diversity appear to play a much less pronounced role in highly complex forest ecosystems. Citation: Zou Y, Sang W, Bai F, Axmacher JC (2013) Relationships between Plant Diversity and the Abundance and a-Diversity of Predatory Ground Beetles (Coleoptera: Carabidae) in a Mature Asian Temperate Forest Ecosystem. PLoS ONE 8(12): e82792. doi:10.1371/journal.pone.0082792 Editor: Dafeng Hui, Tennessee State University, United States of America Received July 31, 2013; Accepted October 29, 2013; Published December 20, 2013 Copyright:  2013 Zou 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. Funding: This research was financially supported by the National Natural Science Foundation of China (31270478), the ‘111 Program’ of the Bureau of China Foreign Experts and the Ministry of Education (2008-B08044) and the Chinese Academy of Science and their Fellowship for International Scientists programme (2011T2S18). The funders 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. * E-mail: swg@ibcas.ac.cn (WS); jan.axmacher@web.de (JCA) resulting in predators catching and feeding on prey more Introduction effectively, so that a higher diversity in the plant community is Terrestrial arthropods play important roles in ecosystem believed to support a higher diversity and abundance also of functioning, for example in pollination, pest control and in predatory species [11,14]. occupying key positions in carbon and nutrient cycling through A positive association between phytodiversity and both diversity food-web links. These roles also strongly impact on plant diversity and abundance of herbivorous arthropods has been found in a patterns [1–4]. Simultaneously, plant species richness is also variety of ecological experiments [4,5,9,15], in low-diversity believed to affect diversity and abundance of arthropods grassland [16–18] and in agriculture fields [19,20]. Nonetheless, throughout the trophic chain via bottom-up effects [5]. An reports of negative relationships between plant diversity and the increase in plant diversity can generally enhance net primary diversity of arthropod taxa are also common, backed again with productivity [6,7], which in term provides more food resources for results from experiments [21], grassland ecosystems [22,23] and herbivorous arthropods, hence increasing the overall biomass of agricultural landscapes [24]. In complex forest ecosystems, a arthropod consumers [8,9]. Apart from this control via food number of studies report a positive feedback between the diversity source effects, arthropod consumers are also known to be of plants and herbivorous insects [25–27]. Other studies nonethe- influenced by top-down control via the abundance of their natural less also report a lack of significant relationships [28,29] or even enemies [10–12]. This control forms the basis of the ‘‘Enemies negative correlations [30,31]. Hypothesis’’ [13], which postulates that species-rich vegetation For studies investigating links between the phytodiversity and assemblages can provide more refuges and more stable prey the diversity and abundance of predatory arthropods, the Enemies availability for predators than plant species-poor assemblages, Hypothesis has been supported by a range of experimental studies PLOS ONE | www.plosone.org 1 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages [5,32–34] and by studies in agricultural [19,35] and grassland [36] [52] ). Of these, 31 plots were sampled both in 2011 and 2012. To ecosystems with relatively low phytodiversity levels. It is predicted increase sampling intensity in the birch forest where overall beetle that top-down control of herbivores by natural enemies would be abundance was very low, two additional birch forest plots were sampled in 2012. more predominant in a perennial ecosystem than annual ones due not least to the more consistent prey availability [21,37]. The associated positive link between plant diversity and the diversity Vegetation Survey and Carabids Sampling and abundance of predatory arthropods is therefore predicted to Each study plot had a size of 20620 m and divided equally be stronger in natural forest ecosystems in comparison to annual into four subplots. In the centre of each sub-plot, a pitfall trap was grassland and agriculture fields. Nonetheless, very little research placed. For the recording of the vegetation, the entire 400 m plot has been conducted to date into these links in the world’s was divided into 4 sub-plots, and all trees and shrubs were remaining mature forest ecosystems. The limited published data recorded in each of the resulting sub-plots. Herbaceous species suggests that areas of high phytodiversity do not automatically were recorded in four plots of 1 m that were randomly located support a high diversity in predatory arthropods [38]. The within each of the sub-plots. The number of individuals was underlying patterns are not yet well-understood, and more studies recorded for each plant species in each layer. The breast height into the links between the vegetation and predatory arthropod area was recorded for each tree specimen and the average height taxa in natural forest ecosystems are urgently needed [39,40]. was recorded for each shrub and herb species. Among important predatory arthropod taxa, ground beetles The pitfall traps for carabid sampling consisted of a 250 ml (Coleoptera: Carabidae) are one of the most species-rich families, plastic cup with an open diameter of 7.5 cm. To minimize the comprising more than 40,000 described species [41]. Members of attractant bias, we used saturated salt (NaCl) water as killing this family, which is chiefly composed of true predators and solution and to preserve specimens in the sampling period [53]. omnivorous species, have been widely used in ecological studies Each cup was filled to about half its volume with saturated salt due to their environmental sensitivity and the good knowledge water, with detergent added to break the water surface tension. base existing in relation to their taxonomy and ecology [41–46]. Above each trap, a solid aluminium roof of 10610 cm was placed Ground beetles are believed to generally benefit from high levels of to protect the solution from dilution and litter contamination. plant diversity [47], and their abundance and diversity is believed Carabids were continually sampled from early July to early August to directly impact on ecosystem functioning [41,48,49]. in 2011 and from late June to late August in 2012, with traps In our study, we used ground beetles as target group to analyse routinely emptied and refilled in about 10 day-intervals. As it was the relationship between abundance and diversity of predatory impossible to sample all plots on the same day due to the large arthropods and phytodiversity. The study was undertaken in one geographical area and other logistical reasons, sampling days of the largest remaining mature temperate forest ecosystems in varied between 22 and 34 for the different plots in 2011, and China. To our knowledge, this is the first study specifically between 42 and 65 days in 2012. focussing on diversity relationship between plants and predatory arthropods in species-rich, mature temperate forests in Asia. Our Data Analysis objectives were 1) to test if positive links between ground beetle Carabid activity abundance of each plot was calculated as the abundance and diversity and the diversity in plant species exist as overall number of sampled individuals divided by the total predicted by the Enemies Hypothesis, and 2) to establish how sampling period in days, resulting in a mean daily catching rate environmental factors affect the observed links. for each plot. Values were calculated for the entire sampling period in 2011 and 2012 to minimize effects of inter-annual Materials and Methods variations. Carabid a-diversity was measured as Fisher’s a,a widely used parametric index considered robust in measuring Ethics arthropod diversity of samples varying in sample size This study was carried out in Changbaishan Nature Reserve [28,31,54,55]. Shannon diversity of the vegetation was calculated and all samplings were permitted by the Changbaishan Nature individually for each plant layer based on the important value (IV) Reserve Management Center. The field study did not involve any of each plant species to avoid the bias from simple abundance- endangered or protected species. based calculations [56,57]. The IV contains three aspects reflecting the relative contributions of each plant species towards Study Area each layer: relative abundance (d), relative frequency (f) and th th Our study area is located on the northern slopes of Changbai relative dominance (h). The IV for i species in j sample plot is Mountain (E 127u439 –128u169;N 41u419 –42u519) in Jilin calculated as: Province, North-eastern China. The local climate is influenced by 0 1 summer monsoon rains. The study area experiences dry, windy spring conditions followed by a short, wet summer, a cool autumn B C 1 d h B i i C with widespread fog and a long, cold winter [50]. The pristine IV ~ z z , i,j B C S S S 3@P P P A forest vegetation is composed of evergreen and deciduous d = h i i coniferous and broad-leaved tree species. The forests on Changbai 1 1 1 Mountain follow a distinctive altitudinal zonation, with a mixed coniferous and broad-leaved forest zone below 1100 m, a mixed where d is the number of individuals, f is the number of subplots in coniferous forest zone between 1100 and 1500 m and a sub-alpine which the species occurred, n is the total number of subplots in a mixed coniferous forest zone between 1500 and 1800 m. The sample plot (4 in this case), and h is the breast height area for tree upper forest boundary is composed of birch forests reaching species and the height for shrub and herb species. elevations of up to 2100 m, followed by a tundra zone with Our modelling of plant-carabid relationships was based on dominating dwarf trees and shrub formations [51]. multiple linear regressions, where carabid activity abundance and We selected a total of 33 plots between altitudes of 700 m and a-diversity were used as response variables, respectively. A series of 2000 m, representing all aforementioned forest types (see details in stepwise linear regression analyses was performed to identify the PLOS ONE | www.plosone.org 2 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages most important independent variables. Stepwise selection was used plots represents the low elevation zone below 1000 m covered by with both forward selection for selection of variables contributing mixed coniferous and broad-leaved forests, while the second significantly (P = 0.05) towards the model and backward elimina- cluster consists of 9 plots located in a median elevation zone tion to verify that variables made no significant contribution in the between 1000 m and 1500 m, containing 3 plots within the mixed selection of new variables. Vegetation variables included the total coniferous and broad-leaved forest type and 6 plots within mixed number of plant species (PS), the Shannon diversity (H) for trees coniferous forests, and the cluster of the remaining 13 plots (TH), shrubs (SH) and herbs (HH), and the abundance density (D) represents the high elevation zone above 1500 m covered by sub- for trees (TD), shrubs (SD) and herbs (HD), respectively. alpine mixed coniferous forests and birch forests. Modelling included all vegetation parameters as independent Below 1000 m in the mixed coniferous and broad-leaved forest variables first and then added elevation as additional independent elevation zone, the first model using vegetation parameters as variable. independent variables indicated that carabid activity abundance To account for the substantial forest vegetation changes with was negatively associated with TH (b = 21.67, P = 0.002) (Table 2, changing elevation, we used Principal Components Analysis (PCA) Model 6, AIC = 5.37, adjusted R = 0.62, F = 17.37, P = 0.002), 2,8 based on the presence-absence data of plant species to establish the while the second model also included a positive relationship with existence of distinct sample clusters representing a relatively SD (b = 0.012, P = 0.012), with a highly significant overall model homogeneous vegetation composition and re-ran the linear fit (Table 2, Model 7, AIC = 21.79, adjusted R = 0.82, regression models separately for the different clusters. F = 23.07, P,0.001). At the intermediate elevation zone, only 2,8 All statistical analysis was carried out in R [58], using the TD (b = 0.002, P = 0.011) was included in predicting carabid packages ‘‘spaa’’ [59] to calculate the Shannon diversity index and activity abundance (Table 2, Model 8, AIC = 14.12, adjusted ‘‘Vegan’’ [60] to carry out the PCA and to calculate Fisher’s a R = 0.57, F = 11.65, P = 0.011). For the highest elevation zone, 1,7 values. SH (b =21.435, P,0.001) was the only independent variable included in the model (Table 2, Model 9, AIC = 21.13, adjusted Results R = 0.73, F = 32.65, P,0.001). 1,11 None of the vegetation diversity variables was significantly We recorded a total of 178 plant species belonging to 128 linked with carabid a-diversity in any of the three distinct elevation genera and 58 families. The tree layer was comprised of 32 species zones. Nonetheless, carabid a-diversity was linked to the belonging to 20 genera and 12 families; the shrub layer contained vegetation density parameters SD (b = 20.058, P = 0.021) at the 43 species of 28 genera and 15 families and the herb layer low elevation zone (Table 2, Model 10, AIC = 21.79, adjusted comprised 112 species representing 88 genera and 43 families. 2 R = 0.40, F = 7.74, P = 0.021) and TD (b = 20.004, P = 0.041) 1,11 Pitfall traps caught 4844 carabids. Ten specimens (0.2%) were not at the high elevation zone (Table 2, Model 11, AIC = 22.41, identified due to substantial damage. The remaining 4834 adjusted R = 0.27, F = 5.37, P = 0.041). Neither herb diversity 1,11 individuals were separated into 34 species and 13 morphospecies. nor herb density appears to be linked to either activity abundance A detailed species list has been provided in [52]. The overall or a-diversity of carabids at any of the three elevation zones. average daily activity abundance for the entire study area was 1.83 individuals per plot. Discussion Carabid-plant Relationships Firstly, our study underlines that changes in elevation were the Stepwise regression entering all vegetation parameters produced predominant drivers of changes in both, carabid abundance and a two subsequent models predicting carabid activity abundance. diversity patterns in CNR, while the overall phytodiversity was not The first model (adjusted R = 0.43, F = 24.63, P,0.001) 1,31 significantly correlated with either abundance or a-diversity of the included SH as significant negative (b =20.925, P,0.001) beetles. Parameters associated with altitudinal changes like predictor of carabid abundance, while the second model (adjusted temperature and precipitation are therefore more important in R = 0.51, F = 17.29, P,0.001) additionally included HH as 2,30 influencing the diversity of ground beetles than plant diversity per positively (b = 0.427, P = 0.02) affecting beetle abundance. The se, which is also consistent with findings for herbivorous insect Akaike information criterion (AIC) slightly decreased from 79.35 diversity patterns [28,29,61,62]. Accordingly, we believe that the to 75.34 (Table 1, Models 1 and 2). The model predicting carabid observed relationships between activity abundance and a-diversity a-diversity again included SH as main predictor (b = 0.571, of carabids and vegetation variables recorded for the entire P = 0.039), which in this case was positively correlated with elevational gradient are mainly driven by the underlying changes Fisher’s a values. Overall, this model performed not as well in the environmental factors. (Table 1, Model 4, adjusted R = 0.10, F = 4.65, AIC = 102.45). 1,31 Nonetheless, the observed, highly significant negative correla- When elevation was entered as additional independent variable, tion between carabid activity abundance and the diversity of MLR models for both, carabid activity abundance and a-diversity, shrubs stands in direct contradiction to the Enemies Hypothesis, only included this parameter as significant, with model fits which predicts a positive relationship with carabid abundance. markedly improved (AIC = 71.71, adjusted R = 0.54, Our observations also stand in contrast to most studies conducted F = 39.13, beta = 1.753, P,0.001, and AIC = 96.27, adjusted 1,31 in agricultural [19,35] and grassland ecosystems [36], which differ R = 0.26, F = 12.11, beta = 21.451, P = 0.002, respectively, 1,31 from our study site by their markedly lower overall phytodiversity. Table 1, Models 3 and 5). Models therefore predict an increased Similar to us, Koricheva et al. [63] also reported a negative beetle abundance at a reduced diversity with increasing elevation. relationship between plant diversity and activity abundance of predatory arthropods in a grassland ecosystem. One of the Carabid-plant Relationship in the Different Vegetation explanations they present for this negative trend was a reduction in Types predator activity density with an increase in herb density, but this The ordination plot of the first two principle components (PCs) trend was not supported by our investigations. However, our based on vegetation composition showed three distinctive clusters results are consistent with observations by Schuldt et al. [38] who along the elevational gradient (Figure 1). A first cluster of eleven observed that activity abundance of spiders was also reduced in PLOS ONE | www.plosone.org 3 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages Table 1. Stepwise linear regression models using activity abundance and Fisher’s a-diversity of carabids as dependent variables, respectively, only using vegetation parameters as independent variables (Model 1, 2 and 4) and including elevation as additional independent variable (Model 3 and 5). Selected Model Adjusted Model independent Std. Error Dependent variable No. R F P-value Model AIC variable(s) b of b t P-value Activity abundance 1 0.43 24.63 ,0.001 79.35 SH 20.925 0.186 24.96 ,0.001 2 0.51 17.29 ,0.001 75.34 SH 20.897 0.173 25.17 ,0.001 HH 0.427 0.174 2.45 0.02 3 0.54 39.13 ,0.001 71.71 ASL(km) 1.753 0.280 6.26 ,0.001 Fisher’s a-diversity 4 0.1 4.65 0.039 102.54 SH 0.571 0.265 2.16 0.039 5 0.26 12.11 0.002 96.27 ASL(km) 21.415 0.530 23.48 0.002 TH: Shannon diversity for trees; SH: Shannon diversity for shurbs: TD: the abundance density for trees; SD: the abundance density for shrubs; Low: low elevation zone of less than 1000 m; Middle: intermediate elevation zone of 1000–1500 m; High: high elevation zone of 1500–2000 m. doi:10.1371/journal.pone.0082792.t001 areas with an increased woody plant diversity in a natural forest in terrestrial ecosystems [68], traditional top-down control theories Zhejiang Province. Schuldt et al. [64] and Vehvila ¨ inen et al. [65] that are suitable in less heterogeneous ecosystems may overall be state that the abundance of predatory species depends more difficult to apply here [39]. strongly on the presence of specific tree species rather than on The reported positive relationship between carabid activity overall tree diversity. The lack of validity of the Enemies abundance and woody plant density at low and intermediate Hypothesis for complex forest ecosystems might therefore relate elevation zones potentially reflects a bottom-up effect: plots with a to the multifaceted interactions between specific plant species, high density in woody plants are likely to be very productive. High their herbivores and the predatory insect assemblages inhabiting woody plant density can not only enhance shading and soil these ecosystems [39,66]. Although we did not investigate the role moisture levels and hence create favourable microhabitats for of specific tree or shrub species and their functional groups, an carabids and their larvae [69], but also producing more leaf litter, increase in woody plant diversity can be linked to either, an which can in term improve soil fertility and increase food availability for carabids [70,71]. The negative correlations increase in their evenness or their species richness, and hence might potentially reflect a reduction in the overall dominance of between woody plant density and the a-diversity of carabids specific favourable species, which could explain the reduction in within low and high elevation forest communities might again relate to changes in arthropod diversity being related to changes in carabid abundance. Alternatively, a high plant diversity can potentially support a higher density of herbivorous arthropods in the woody plant species composition, rather than their overall natural forests [25–27,67], which might also result in a reduction diversity [23,72]. Additionally, impacts of plant diversity are known to decrease with increasing trophic levels [5,73], so that of predators’ overall foraging time and hence their recorded activity density [38]. An increased plant diversity and the impacts of the vegetation on the diversity of predatory insects is often quite complex. associated assumed increase in herbivores can furthermore The negative relationship between altitude and the a-diversity provide an increase in food sources and niches for competing predatory arthropod taxa such as spiders and ants, increasing the of carabids can be explained by the Harsh Environmental overall competition levels for prey and consequently reducing the Hypothesis. Accordingly, species at high altitudes experience overall abundance of carabids. As food chains and habitats are harsh climatic conditions requiring them to have broader overall much more complex in forests in comparison to most other tolerance ranges than species at low altitudes, which in term leads to wider distribution ranges with increasing elevation and to a higher species richness at low altitudes [74–76]. This hypothesis is supported by the observed increase in carabid species’ altitudinal ranges with increasing elevation that we previously reported [52]. A possible reason for the positive links between carabid activity abundance and elevation could be the reduction of competitors such as ants and other predatory arthropods [77] or changes in the activity patterns due to potential scarcity of food resources, which would also increase the number of specimens sampled at high altitudes. Our results finally showed that the density of herbaceous plants did not significantly influence carabid activity abundance nor their diversity, which stands in strong contrast to studies in grassland ecosystems that commonly record negative relationships [78–80]. Pitfall traps have been widely used in surveys of ground-dwelling Figure 1. PCA ordination plot based on vegetation composi- arthropods [42,78,81–84] and can be considered as a standard tion showing three distinct clusters (proportion variance method in ground beetle sampling [42]. Nonetheless, one of the explained for PC1 = 24% and for PC2 = 11%; eigenvalues for main known pitfalls of pitfall trapping is the dependency of the PC1 = 4.83 and PC2 = 2.12). doi:10.1371/journal.pone.0082792.g001 sampling rate on both the target population density and the PLOS ONE | www.plosone.org 4 December 2013 | Volume 8 | Issue 12 | e82792 Vegetation Affects Carabid Assemblages Table 2. Results of stepwise linear regressions for the three elevational zones using activity abundance and Fisher’s a-diversity of carabids as dependent variables and vegetation parameters as independent variables. Selected Elevation Model Adjusted Model Model independent Std. Error Dependent variable zone No. R F P-value AIC variable(s) b of b tP-value Activity abundance Low 6 0.62 17.37 0.002 5.37 TH 21.670 0.401 24.17 0.002 7 0.82 23.07 ,0.001 21.79 TH 21.236 0.310 23.99 0.004 SD 0.012 0.004 3.24 0.012 Middle 8 0.57 11.65 0.011 14.12 TD 0.012 0.003 3.41 0.011 High 9 0.73 32.65 ,0.001 21.13 SH 21.435 0.251 25.71 ,0.001 Fisher’s a-diversity Low 10 0.40 7.74 0.021 21.79 SD 20.058 0.021 22.78 0.021 High 11 0.27 5.37 0.041 22.41 TD 20.004 0.157 22.32 0.041 TH: Shannon diversity for trees; SH: Shannon diversity for shurbs: TD: the abundance density for trees; SD: the abundance density for shrubs; Low: low elevation zone of less than 1000 m; Middle: intermediate elevation zone of 1000–1500 m; High: high elevation zone of 1500–2000 m. doi:10.1371/journal.pone.0082792.t002 individual specimen’s activity [78,85–87]. Factors affecting this China, such as Liangshui and Fenglin Natural Reserve in activity need to be taken into consideration when comparing pitfall Heilongjiang Province, are ideal study areas to substantiate results samples, and it has commonly been suggested that vegetation from species-rich temperate forests. These latter studies in some of density particularly of herbaceous species needs to be considered the last remaining highly diverse mature temperate forest in the respective data interpretation [79,80]. The negative impact ecosystems in NE China would also allow a better understanding of this density in grassland ecosystems is believed to be due to a of the complex inter-linkages between taxa and across trophic reduction in the ground beetle mobility caused directly by a dense levels, with particular foci on the role of the woody plant species herb layer [79,80]. However, our results strongly suggest that the composition on predator distribution patterns and on the density of this layer in the old-growth forests on Changbai mechanisms governing responses of herbivorous arthropods to Mountain is not dense enough to significantly affect carabids’ changes in plant diversity and species composition. movements, supporting the argument that the influence of the density in understory vegetation can be neglected when studying Acknowledgments forest carabid assemblages [38]. Nonetheless, controlled capture- We thank Professor Liang Hongbin and his group at the Institute of recapture experiments would be needed to evaluate the exact Zoology, Chinese Academy of Sciences for their great help with carabid effects which might be present. identification. We are also grateful for the kind support from the Overall, our results clearly indicate that, in highly complex Changbaishan Forest Ecosystem Research Station, the Changbaishan forest ecosystems, predatory arthropod abundance and diversity Nature Reserve Management Center, the Changbaishan Academy of patterns do not support traditional top-down control theories that Sciences and the Changbaishan Natural Museum. We also greatly appreciate the help with our fieldwork from Eleanor Warren-Thomas, are suitable for less complex ecosystems. To substantiate these Long Chao, Liu Min, Zhou Xiasai and Han Furen. conclusions and establish if the Enemies Hypothesis is generally unsuitable for complex forest ecosystem, we suggest long-term Author Contributions monitoring of a wider range of predatory arthropod groups (e.g. spiders, ants and centipedes) not only in temperate, but also in Conceived and designed the experiments: YZ WS FB JCA. 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