Ground Beetle (Coleoptera: Carabidae) Diversity and Body-Size

Ground Beetle (Coleoptera: Carabidae) Diversity and Body-Size Variation in Four Land Use Types in a Mountainous Area Near Beijing, China Author(s): Xin Zhang, Guishen Zhao, Xuzhu Zhang, Xiao Li, Zhenrong Yu, Yunhui Liu and Hongbin Liang Source: The Coleopterists Bulletin, 71(2):402-412. Published By: The Coleopterists Society https://doi.org/10.1649/0010-065X-71.2.402 URL: http://www.bioone.org/doi/full/10.1649/0010-065X-71.2.402

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. The Coleopterists Bulletin, 71(2): 402–412. 2017.

GROUND BEETLE (COLEOPTERA:CARABIDAE)DIVERSITY AND BODY-SIZE VARIATION IN FOUR LAND USE TYPES IN A MOUNTAINOUS AREA NEAR BEIJING,CHINA

XIN ZHANG,GUISHEN ZHAO,XUZHU ZHANG,XIAO LI,ZHENRONG YU,YUNHUI LIU College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, CHINA [email protected]

AND

HONGBIN LIANG Institute of Zoology, China Academy of Science, Beijing 100101, CHINA [email protected]

ABSTRACT Mountainous areas are characterized by high biological diversity but are threatened by agricultural reclamation. To evaluate the effects of agricultural land use and woody crop intercropping on carabid diversity in mountainous regions, we compared the diversity of carabid beetles and their body size compositions in two walnut plantations (monoculture and newly established intercropping system) and two secondary succession habitats (secondary forest and grassland) in 2011 and 2012. Carabid activity-abundance did not differ among the walnut plantations and secondary succession habitats for both sampling years, and species richness was higher in the walnut monoculture in 2012. However, the secondary succession habitats harbored more large carabid individuals than the walnut plantations. All of the carabid species compositions in the walnut plantations differed from those in the secondary succession habitats, whereas the species compositions of large carabids in the walnut plantations differed from those in the secondary succession habitats in 2012 but were similar in 2011. We conclude that converting secondary succession lands to walnut plantations had little effect on both the alpha diversity and species turnover of carabid assemblages, but the secondary succession lands were essential for sustaining diverse large carabids, which comprised conserved species and natural control agents. The newly introduced walnut-chrysanthemum intercropping system did not produce significant short-term losses in carabid diversity compared with the walnut monoculture system, but the concept that the walnut-chrysanthemum intercropping system could serve as a trade-off between production and biodiversity conservation will require long-term monitoring.

Key Words: ground beetles, biodiversity conservation, land use change, intercropping, woody crop

DOI.org/10.1649/0010-065X-71.2.402

Mountainous areas are characterized by high (Fu et al. 2006a,b) and changes in biodiversity biological diversity because they contain a high (Menon and Bawa 1997; MacDonald et al. 2000; concentration of environmental gradients and Mitchley et al. 2006), have been essential for habitat heterogeneity (Myers et al. 2000; K¨orner monitoring the sustainability of agricultural land et al. 2005; Spehn et al. 2010). This high diversity in reclamation in mountainous areas. According to mountainous areas has great potential in terms of earlier studies in plains across the world, land use biodiversity conservation. Mountains are estimated changes resulting from agricultural production lead to support approximately one-quarter of the world’s to a loss of biodiversity (Reidsma et al. 2006; terrestrial biodiversity and include nearly half of the Trisurat et al. 2010) and changes in functional world’s biodiversity “hotspots” (Myers et al. 2000; composition (Clavel et al. 2011; Tscharntke et al. Myers and Kent 2004). 2012) that could potentially lead to a decline in Unfortunately, many mountainous lands are ecological services essential for sustainable devel- reclaimed for agricultural production in developing opment (Ostfeld and Logiudice 2003; Gagic et al. countries to feed the increasing human population 2012). However, plantations diversified by inter- (Li and Wang 2003; Mitchley et al. 2006). Woody cropping a woody cash crop with other crops cash crops, mainly fruit or nut trees, are commonly could serve as an efficient way to conserve local selected for plantations as a compromise between biodiversity via agricultural management (Doblas- improving the local livelihood and keeping as much Miranda et al. 2014; Gibbs et al. 2016). This raises perennial vegetation cover as possible. Environ- the question of whether woody cropping or woody mental evaluations, including soil and water erosion crop-based intercropping systems would result in

402 THE COLEOPTERISTS BULLETIN 71(2), 2017 403 substantial changes in the functional composition successional lands were reclaimed for walnut and loss of biodiversity and how biodiversity in the plantations. Recently, a creative agroforestry sys- mountainous region would be impacted by such an tem, in which chrysanthemum and walnut were agricultural strategy. The answers to these questions intercropped on the plantation, was developed for are the foundation for developing an approach that sightseeing as an example of a prosperous plantation balances biodiversity conservation with the pro- for agritourists. The sampling plots were located at duction of substantial economic commodities to Puwa Town (E115° 350 – 115° 460, N39° 430 – 39° improve local livelihoods (Mitchley et al. 2006). 490) with an elevation range of 407 to 1,870 m. Carabid beetles (Coleoptera: Carabidae) are im- The town is dominated by natural secondary portant predators in agroecosystems (Holland forest, primarily composed of Quercus liaotungensis 2002). We investigated the diversity of Carabidae in Koidz (Fagaceae), Carpinus turczaninowii Hance habitats of different land use types in the moun- (Betulaceae), Platycladus orientalis (L.) Franco tainous area of Beijing to evaluate the beetles’ re- (Cupressaceae), Populus davidiana Dode (Salica- sponses to land use changes. These beetles are ceae), and Juglans mandshurica Maximowicz relatively well known taxonomically and ecologi- (Juglandaceae); the remaining habitats are com- cally, suitable for standardized sampling, and are prised of brush land (31%), alpine meadow (10%) sensitive to environmental changes (L¨ovei and and secondary forest (3%). Because the high Sunderland 1996; Rainio and Niemel¨a 2003). proportion of secondary forest serves as an im- However, there are highly divergent ecological traits portant habitat for Red List plants (such as Tilia within the family that would result in varied re- amurensis Rupr. (Tiliaceae), Phellodendron amur- sponses to anthropogenic disturbances (Purtauf ense Rupr. (Rutaceae),andGlycine soja (Siebold et al. 2005; Gobbi and Fontaneto 2008). Therefore, and Zucc.) (Fabaceae)), Red List birds (Cross- it could be important to incorporate carabid func- optilon mantchuricum Swinhoe), and the local tional traits (such as wing morphology, diet, and endangered Chinese bee (Apis cerana Fabricius), body size) into analyses for a more accurate as- the town was designated as a nature reserve of sessment of the impacts of land use changes (Purtauf Beijing in 2005. In addition to secondary suc- et al. 2005; Gobbi and Fontaneto 2008). We made cessional vegetation cover, there were 227 ha of the following hypotheses: 1) converting secondary farmland, which accounted for 2.48% of the total forests and natural succession meadows to walnut area, and 50 ha of walnut forests in Puwa Town. plantations would significantly change the carabid Walnut monoculture systems were introduced in body-size composition; 2) both walnut mono- the early 1990s. The walnut-chrysanthemum system culture and walnut-chrysanthemum intercropping was created in 2011 by planting 11 chrysanthemum systems would sustain less biodiversity and have varieties of six colors under established walnut trees smaller species than the more natural habitats; and to form a unique chrysanthemum terrace landscape 3) a walnut-chrysanthemum intercropping system that was intended to attract tourists and increase would sustain greater biodiversity than a walnut the output per unit area. Chemical fertilizer (diam- monoculture system. Finally, we further explored monium phosphate) and NPK compound-fertilizer (N:P: how changes in carabid biodiversity relate to en- K 5 28:6:6) and green manure were used one or two vironmental variables in different land use types to times in the spring. Pesticides (cypermethrin) were enable a deeper understanding of how carabids used at least once to control walnut pests (Myzus respondtolandusechanges. persicae (Sulzer)) during the sampling season. Carabid Sampling. To evaluate the potential effects of changes in land use on local carabid MATERIAL AND METHODS biodiversity, two planting habitats, a walnut Study Area. The study area was located near monoculture system (Juglans regia L.) and walnut- Puwa Town in the Fangshan District southwest of chrysanthemum intercropping system, and two Beijing, China. The locale has a semi-humid con- secondary successional habitats, secondary tem- tinental monsoon climate, with an annual temperate deciduous forest (consisting of larch trees perature of ;10.8°C and an average annual (Larix principis-rupprechtii Mayr; Pinaceae)) and precipitation of ;645.2 mm. More than 72% of alpine meadow, were selected. Four spatially Fangshan District is mountainous and mainly distinct replicate plots were selected for each covered with forest and naturally successional al- habitat, which varied in elevation and were located pine meadow. Because of long-term human activity at least 50 m away from neighboring plots. In each and disturbances in the region, little pristine forest plot, five pitfall traps were placed 5 m from remains; most forests are secondary forest, which neighboring traps in a straight line at the center of were mainly formed in the 1970s after a large area of each plot. The pitfall traps consisted of plastic deforestation during the Steel Movement in the beakers 8 cm in diameter and 11.5 cm in height and 1950s. In the late 1990s, some of these secondary were protected from rain by a simple aluminum 404 THE COLEOPTERISTS BULLETIN 71(2), 2017

roof positioned approximately 5 cm above the trap. where Bi represents the mean body size of each The pitfall traps were partially filled with 75% species, Ni represents the number of individuals of alcohol to kill and preserve the collected specimens the species i in each plot, and n is the total number of (Southwood 1978). From 2011 to 2012, all pitfall carabid species in each plot. traps were in the field for six days every month from June to September. Specimens caught in the same plot during the sampling season were pooled RESULTS for statistical analysis. Species Composition and Alpha Diversity. A The body size of each individual specimen, total of 634 carabids representing 11 genera and 28 measured as the distance from the anterior margin of species were collected at all sampling plots over a the labrum to the apex of the abdomen, was recorded sampling period of 2 years (Table 1). Among these, with a precision of 1 mm using a Vernier Caliper. 225 individuals representing 18 species were found Based on the measurement of five individuals (if in the walnut planting habitats, and 260 individuals there were more than five individuals) or all of each representing 18 species occurred in the secondary species (if less than five), the average body size was successional habitats (Table 1). calculated. Following Cole et al. (2002), all species The carabid assemblages were strongly domi- that reached an average length of at least 15 mm nated by three species: Harpalus griseus (Panzer) were classified as large species. (,15 mm), Carabus vladimirskyi (Dejean) (.15 mm), Recording of Environmental Parameters. At and Pterostichus fortipes (Chaudoir) (,15 mm), each plot, vegetation was characterized by plant which accounted for 60.3% of all captured in- species richness and the total percentage cover of all dividuals. Among these three species, 29.8% of plants in four randomly selected 1 m 3 1 m quadrats the individuals were H. griseus species (n 5 189), in July 2012. To characterize soil properties, four which were primarily found in the walnut mono- samples were randomly taken from the upper 20 cm culture and walnut-chrysanthemum intercropping of the mineral soil on each plot and mixed prior to systems. Secondary forest and alpine meadow analysis in August 2011. Soil organic matter, total habitats were characterized by high abundances nitrogen, total phosphorus, and pH values were (17.2%) of C. vladimirskyi (n 5 109). Pterostichus subsequently tested using National Standard fortipes (n 5 84) was the third most dominant Methods (NY/T 2006). species (13.3%), which was primarily found in the Data Analysis. Activity-abundance (individuals forest. per pitfall trap per day) and estimated species There were 44 carabid individuals representing richness (Chao1) in individual plots were used for eight species that were only found in the two suc- analysis to avoid differences in sampling efforts due cessional habitats, and another 79 carabid individuals to the occasional loss of a pitfall trap. Chao1 was representing 10 species were only found in the calculated using PAST 3.08 (Hammer et al. 2001). walnut planting habitats (Table 1). Nine species A one-way analysis of variance was performed (represented by 210 individuals) were large species using the Data Processing System v7.05 (Tang and and accounted for 33.1% of total individuals. More Feng 1997, 2002) to establish differences among than 74% of the large species individuals were habitats in terms of activity-abundance and rarefied present in the two secondary successional habitats, species numbers for the largest common sample whereas more than 76% of the species that were less size. than 15 mm long occurred in the walnut planting Non-metric multidimensional scaling based on habitats. Among the species that were solely present Euclidean distances was applied to analyze the in more natural habitats, 70.5% of the individuals (of species turnover rates of carabid groups among sites two species) were large species. We found a greater using PAST (Hammer et al. 2001). Canonical average body size for carabid assemblages in the secondary successional habitats than in the walnut correlation analysis (CCA) was applied to explore 5 , relationships between environmental parameters plantations (F 21.81; p 0.01) (Table 1). and the composition of carabid assemblages using Alpha Diversity. There was no difference in the activity-abundance of carabid assemblages for any Canoco 5.0 for Windows (Ter Braak and Smilauerˇ habitat in 2011 (F 5 2.82, p 5 0.08) and 2012 (F 5 2012). The average body size (S) of the carabid 2.58, p 5 0.10) (Fig. 1a). Estimated species richness community in each plot was calculated using the was not significantly different among habitats in following formula: 2011 (F 5 0.96, p 5 0.44); in 2012, the walnut n monoculture system held a greater value than that of å B 3 N 5 , S ¼ i ¼ 1 i i all other habitats (F 6.32, p 0.01) (Fig. 1b). ån The activity-abundance of large carabids (.15 mm) i ¼ 1Ni did not differ among habitats in 2011 (F 5 0.87, THE COLEOPTERISTS BULLETIN 71(2), 2017 405

Table 1. Species, mean body size, and number of captured individuals of carabid beetles in four habitats near Puwa, Fangshan, Beijing, China in 2011 and 2012. WI 5 walnut-chrysanthemum intercropping system; WM 5 walnut monoculture system; F5 temperate deciduous forest; M 5 alpine meadow; 15species only found in natural habitat; * 5 species only found in walnut-planted habitats.

Habitat Body size Species (mm) WI WM F M Total S1 Amara alacris Tschitscherine, 1899* 5.8 - 1 - - 1 S2 Amara communis (Panzer, 1797)1 7.3 - - 2 - 2 S3 Amara vagans Tschitscherine, 1897* 7.9 4 - - - 4 S4 Carabus brandti Faldermann, 18351 27.4 - - - 2 2 S5 Carabus manifestus (Kraatz, 1881)1 21.0 - - 17 12 29 S6 Carabus smaragdinus Fisher, 1823 33.6 2 - 2 6 10 S7 Carabus vladimirskyi (Dejean, 1830) 22.9 2 1 66 40 109 S8 Curtonotus giganteus (Motschulsky, 21.3 5 7 1 1 14 1844) S9 Curtonotus macronota Solsky, 1875 13.2 8 21 3 - 32 S10 Dolichus halensis (Schaller, 1783) 17.6 4 12 4 - 20 S11 Harpalus bungii Chaudoir, 1844* 8.6 6 13 - - 19 S12 Harpalus calceatus (Duftschmid, 13.8 3 8 - - 11 1812)* S13 Harpalus coreanus (Tschitscherine, 14.4 - 1 - - 1 1895)* S14 Harpalus corporosus (Motschulsky, 15.0 2 7 - - 9 1861)* S15 Harpalus crates Bates, 1873* 12.6 - 1 - - 1 S16 Harpalus griseus (Panzer, 1797) 11.3 98 84 - 7 189 S17 Harpalus pallidipennis Morawitz, 1862 10.1 - 5 - 1 6 S18 Harpalus pastor Motschulsky, 1844 11.4 14 20 2 4 39 S19 Harpalus rubripes (Duftschmid, 13.4 - - - 1 1 1812)1 S20 Harpalus simplicidens Schaubeger, 12.7 - 22 - - 22 1929* S21 Oxycentrus melas (Schmidt-G¨obel, 8.3 - - - 1 1 1846)1 S22 Pristosia sp.1 13.8 - - 1 1 2 S23 Pterostichus fortipes (Chaudoir, 1844) 14.4 1 9 59 15 84 S24 Pterostichus gebleri Dejean, 1828* 17.9 - 10 - - 10 S25 Synuchus major Lindroth, 19561 8.2 - - 1 - 1 S26 Synuchus nordmanni (Morawitz, 9.3 - - 5 1 6 1862)1 S27 Tachys gradatus Bates, 1873* 3.0 - 1 - - 1 S28 Trigonognatha jaechi Sciaky, 1995 22.2 - 2 2 3 7 Average body size of carabid (mm)1 13.261.8b 12.860.7b 18.561.9a 20.862.1a

1 Means of body size for individuals from each habitat followed by the same letter are not significantly different (p . 0.05). p 5 0.50) (Fig. 1c), but it was greater in the sec- between the forest and meadow plots or between ondary successional habitats than in the walnut the two walnut planting habitats in either year planting habitats (F 5 6.35, p , 0.01) in 2012. (Fig. 2a, b). However, the estimated species richness did not For large carabids (Fig. 2c, d), all plots were differ among habitats in either year (2011: F 5 0.98, closely clustered with the exception of three plots p 5 0.04; 2012: F 5 2.08, p 5 0.16) (Fig. 1d). in 2011, indicating a relatively homogeneous Species Turnover. Non-linear two-dimensional composition of large carabid species across the scaling of carabid assemblages based on Euclid- habitats. However, plots of the walnut planting and ean measures showed that the species composi- secondary successional habitats were more clearly tions in both walnut planting habitats were distinct delineated in 2012. This indicated a more hetero- from the species compositions in the natural geneous composition of large carabid species be- secondary habitats in both 2011 and 2012 (Fig. 2a, tween walnut plantation and natural secondary b). In contrast, there were no distinct differences habitats for the second year. Again, there were no 406 THE COLEOPTERISTS BULLETIN 71(2), 2017

Fig. 1. Activity-abundance and species richness of Carabidae in four habitats in a mountainous area near Beijing, China in 2011 and 2012. a) Activity-abundance of all carabids (2011: F 5 2.82, p 5 0.08; 2012: F 5 2.58, p 5 0.10), b) Chao1 index for all carabids (2011: F 5 0.96, p 5 0.44; 2012: F 5 6.32, p , 0.01), c) Activity-abundance of large carabids (2011: F 5 0.87, p 5 0.50; 2012: F 5 6.35, p , 0.01), d) Chao1 index for large carabids (2011: F 5 0.98, p 5 0.04; 2012: F 5 2.08, p 5 0.16) WI 5 walnut-chrysanthemum intercropping system; WM 5 walnut monoculture system; F 5 temperate deciduous forest; M 5 alpine meadow. Bars within each year of each graph with the same letter above the standard error bar are not significantly different ( p . 0.05). distinct differences between the forest and meadow on the biplot. The temperate deciduous forest and plots or between the two walnut planting habitats for alpine meadow distributed on the right side of the either year (Fig. 2c, d). biplot showed a stronger association with higher soil Species-Environment Relationships. The ca- organic matter content, plant cover, and soil nitro- nonical correspondence analysis of six environ- gen content. The walnut planting systems were mental parameters resulted in eigenvalues of 0.59 located on the left side of the biplot, indicating that and 0.25 for the first and second axes, respectively. these habitats have higher soil pH and phosphorus The first and second axis explained 27.8% and content. 11.6%, respectively, of the total variance in the In the ordination diagram, when the species and dataset. Monte Carlo tests for the first canonical axis environmental arrows point in the same direction, (F 5 3.46, p , 0.01) and all canonical axes (F 5 species are predicted to have a large positive cor- 2.19, p , 0.01) were significant. relation with the environmental variable, whereas if According to the CCA biplot, plant coverage, the species and environmental arrows point at op- total soil nitrogen content, soil organic matter posite directions, species are predicted to have a content, soil pH, and total soil phosphorus content large negative correlation with the environmental were strongly correlated with the first canonical variable. As Fig. 3 shows, 12 species (S2, S4, S5, axis, whereas only plant coverage and total soil S6, S7, S19, S21, S22, S23, S25, S26, and S28, see nitrogen content showed strong correlations with Table 1 for species names) were distributed on the the second axis. Plots showed distinct distributions right side of the first axis, indicating that the THE COLEOPTERISTS BULLETIN 71(2), 2017 407

Fig. 2. Non-linear two-dimensional scaling of carabid samples based on Euclidean distance. a) All carabids in 2011, b) all carabids in 2012, c) large carabids in 2011, d) large carabids in 2012. WI 5 walnut-chrysanthemum intercropping system; WM 5 walnut monoculture system; F 5 temperate deciduous forest; M: alpine meadow. occurrence of these species was strongly associated of large carabid species and large carabid in- with high plant coverage, soil organic matter con- dividuals, respectively, and were primarily pres- tent, and total soil nitrogen content, but low soil pH ent in walnut planting systems (Table 1, Fig. 3). and soil total phosphorus content. Among the 12 Additionally, Amara alacris Tschitscherine, species, Carabus brandti Faldermann, Carabus Harpalus calceatus (Duftschmid), Harpalus manifestus (Kraatz), Carabus smaragdinus Fisher, coreanus Tschitscherine, and Harpalus crates C. vladimirskyi, and Trigonognatha jaechi Sciaky Bates have greater positive values on the second were large species, accounting for more than 55.6% axis, indicating their strong correlation with plots and 86.7% of the large carabid species and large with higher plant coverage but lower total soil nitrogen content. However, Oxycentrus melas carabid individuals, respectively. These individuals Schmidt-G¨obel has a greater negative value on the were primarily present in the secondary succes- second axis, indicating its strong association with sional habitats (Table 1, Fig. 3). The other 16 species plots of lower plant coverage but greater total soil were distributed on the left side of the first axis, nitrogen content (Fig. 3). indicating their occurrence in plots with higher soil pH and total phosphorus content (walnut planting plots). Four of these 16 species (Curtonotus giganteus (Motschulsky), Dolichus halensis (Schaller), Harpalus DISCUSSION corporosus (Motschulsky), and Pterostichus gebleri Transformations of natural or semi-natural hab- Dejean) were large carabid species. These species itats into agricultural land have become an impor- accounted for the remaining 44.4% and 13.3% tant cause of biodiversity loss (Foley et al. 2005; 408 THE COLEOPTERISTS BULLETIN 71(2), 2017

necessarily related to decreases in the alpha diversity of carabid assemblages and could even encourage greater beta diversity by creating a more heterogeneous landscape mosaic. This is consistent with earlier studies that found that the replacement of forest habitat by land use systems that retain dense and diverse canopies of shade trees (e.g., agroforestry systems) was likely to have a less negative impact on at least some components of biodiversity compared with the conversion of forests to land use types that dramatically simplify and modify the vegetative composition and structure, such as open pastures or crop monocultures (Estrada et al. 1993, 1998; Greenberg et al. 1997; Schroth et al. 2004). The comparable alpha diversity in the walnut planting habitats (observed in the secondary successional habitats despite more frequent anthropogenic disturbances) could be due to the fol- Fig. 3. Canonical correspondence analysis of lowing reasons. On one hand, an agroforestry carabid beetles (for species names, refer to Table 1), system may harbor more insect diversity by pro- sample plots, and environmental parameters. N 5 soil viding more food resources due to its high pro- total nitrogen content; P 5 soil total phosphorus ductivity (Tscharntke et al. 2005; Burgess et al. content; OM 5 soil organic matter content; pH 5 soil 2007; Clough et al. 2011; Smith et al. 2014). On the pH; PC 5 plant coverage; PS 5 plant species; WI 5 other hand, microclimatic or local habitat conditions walnut-chrysanthemum intercropping system; WM 5 5 in agroforestry systems may favor certain species walnut monoculture system; F temperate deciduous (Bos et al. 2008; Sporn et al. 2009; Seibold et al. forest; M: alpine meadow. 2016). For example, the relatively open environment in walnut planting systems could favor some species, and the lower contents of soil nitrogen and Alkemade et al. 2009; Pereira et al. 2010). In organic matter and greater soil phosphorus content contrast to our hypothesis that the walnut planting and pH in walnut planting systems may be favored system would have lower carabid diversity than the by some species. Ordination analysis demonstrated secondary successional habitats, greater carabid that the substantial differences in species compo- species richness was observed in the walnut sition between natural and planting habitats were monoculture systems compared with the walnut associated with environmental variables such as intercropping systems and both secondary succes- plant coverage, plant species, and soil properties. In sional habitats in 2012, but carabid activity- addition, because the pristine vegetation of the re- abundance and species richness were comparable gion had suffered from destruction during the last between both walnut planting habitats in 2011. century, the current persistent carabids would be Despite a lack of significant differences in alpha those that were more able to adapt to human dis- diversity among carabid assemblages, our study turbances and open environments. found distinct species compositions of carabid as- Consistent with our expectations, walnut plan- semblages between the secondary successional tations harbored more small species than the sec- habitats and the walnut planting systems. This was ondary successional habitats, and their carabid further demonstrated by observing unique and assemblages had substantially smaller average sizes dominant species. For example, H. griseus (a small compared with the two natural habitats. As earlier species), which was primarily collected in walnut studies have indicated, large species are more intercropping and walnut monoculture systems, susceptible to anthropogenic disturbances due to accounted for 96.3% of the total individuals in these their lower reproductive output, longer larval stages, habitats. However, C. vladimirskyi (a large species) and reduced dispersal abilities (Blake et al. 1994; primarily appeared in forest and meadow systems Kotze and O’Hara 2003; L¨ovei and Magura 2006). and accounted for 97.2% of the total individuals in In our study, large carabids, including C. brandti, these habitats. C. manifestus, C. smaragdinus, C.vladimirskyi, and Interestingly, more carabid species were found T. jaechi, were all significantly negatively related to only in walnut planting habitats than only in sec- environmental variables, including pH and soil ondary successional habitats (10 vs. 8), indicating phosphorus content, which were greater in the that transformations of secondary successional walnut planting systems than in natural habitats habitats into walnut planting systems were not (Table 2). These variables are reported to be THE COLEOPTERISTS BULLETIN 71(2), 2017 409 closely linked to fertilizer application (Bosak and species richness, or species composition of Cara- Smeyanovich 2003; Cai et al. 2011). Our obser- bidae and that the diversities were comparable to vation may be explained by the secondary succes- those in more natural lands. Chrysanthemum inter- sional habitats because they were less disturbed by cropping did not appear to significantly improve alpha fertilization and harvesting activity. The successional and beta diversity in the walnut agroforestry system; habitats could favor, therefore, a greater abundance however, whether the walnut-chrysanthemum inter- of these large carabids than walnut planting systems, cropping system could be an efficient method for particularly for species of the genus Carabus Lin- improving local production and economic benefits naeus, which is the most common genus of large without compromising biodiversity still requires a Carabidae among the conserved species in China (Yu long-term evaluation. Given the changes we observed et al. 2001). Our study also indicated that changing in carabid species richness and the large species secondary successional mountain habitat into walnut composition between the two sampling years, coupled planting systems would drive the loss of large ca- with the potential negative effects of the introduction rabids or change the composition of large species, of agritourism, the walnut-chrysanthemum inter- which could result in the loss of their associated cropping system could have negative effects on biological services since most large carabids are biodiversity (Wu et al. 2006; Bruci et al. 2012). predators (Liu et al. 2015). Furthermore, our results Our results showed that the alpha diversity of confirmed the argument that a general analysis of carabids in walnut planting systems is similar to that assemblage diversity could be misinterpreted, and it in secondary successional habitats, but species is important to include functional traits in evaluating composition was distinct between the walnut and monitoring the effect of human impacts on ca- planting habitats and secondary successional hab- rabid species assemblages (Gobbi and Fontaneto itats. The walnut agroforest system harbored fewer 2008). As our study indicated, body size is a func- large carabid beetles than the secondary successional tional trait that could be included for more efficient forest and alpine meadow. Walnut-chrysanthemum evaluation and monitoring of the effect of human intercropping showed no significant changes in activities on the environment when carabid beetles species richness or species composition hetero- are used as bioindicators (Aviron et al. 2005; Liu geneity compared to walnut monoculture. And et al. 2012). the conversion of secondary forests and alpine The most common goal of intercropping is to meadows into walnut planting systems had little produce greater yields on a given plot of land by effect on the overall alpha diversity of carabid utilizing resources that would not otherwise be assemblages but could have negative effects on available for a single crop (Hawke and Percival larger-sized carabids, which could be further 1984; Bhagwat et al. 2008). Recent studies have detrimental to biological control functions and also suggested that intercropping could provide conserved species in the region. Changes in the important trade-offs between biodiversity conser- soil and plant variables may explain the changes vation and agricultural production (Bhagwat et al. in species composition. A high level of carabid 2008; Clough et al. 2011). In our study, the walnut- gamma diversity requires a landscape mosaic chrysanthemum intercropping system was primarily utilizing both walnut planting systems as well as developed for both sightseeing and greater yields. secondary forests and meadows in the region. With the 2012 opening of a sightseeing site in the Furthermore, whether the development of the study region, chrysanthemums provided additional diversified walnut planting system intercropped value to the walnut planting system, including those with chrysanthemum could serve as an effective related to tourism, food, and medicine. Our in- measure for improving both production yields vestigation found that walnut monoculture and and economic income without loss of diversity intercropping did not change the activity density, requires long-term monitoring.

Table 2. Soil properties and vegetation cover in sampling habitats. WI 5 walnut-chrysanthemum intercropping system; WM 5 walnut monoculture system; F 5 temperate deciduous forest; M 5 alpine meadow; N 5 nitrogen content of the soil; P 5 phosphorus content of the soil; OM 5 organic matter content of the soil.

Variable WI WM F M N (%) 0.1860.02 0.1660.04 0.2360.03 0.2860.11 P (%) 0.0360.01 0.0360.005 0.0160.01 0.0260.01 OM (%) 3.9660.53 3.9660.53 4.8160.63 5.4961.67 pH 6.2060.18 6.4360.32 5.7860.18 5.7660.18 Plant Species 26.50613.23 33.5061.73 34.0066.06 32.5067.33 Plant Cover (%) 73.6362.43 75.63614.20 90.8863.12 88.0064.69 410 THE COLEOPTERISTS BULLETIN 71(2), 2017

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