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Temporary non-crop habitats within arable fields: The effects of field defects on carabid beetle assemblages
Agriculture, Ecosystems and Environment 293 (2020) 106856
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Temporary non-crop habitats within arable fields: The effects of field defects on carabid beetle assemblages
T
Miroslav Seidla, Ezequiel Gonzáleza, Tomáš Kadleca, Pavel Saskaa,b, Michal Knappa,* a b
Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague - Suchdol, 165 00, Czech Republic Crop Research Institute, Drnovská 507, Prague 6 - Ruzyně, 161 06, Czech Republic
A R T I C LE I N FO
A B S T R A C T
Keywords: Agri-environmental schemes Agricultural landscape Biodiversity Carabidae Ecosystem services Ephemeral habitats Oilseed rape
Landscape heterogeneity and higher complexity generally increase biodiversity in agroecosystems. Carabid beetles represent abundant and important predators of pests and weed seeds in temperate agroecosystems and are affected by landscape structure. Several studies have described the impact of permanent non-crop habitats such as woodlots, hedgerows, and grassy margins on carabid assemblages. However, temporal non-crop habitat islands within arable fields have been rarely investigated. The aim of this study was to investigate spatial distribution of carabid beetles within oilseed rape fields having temporary non-crop habitats (field defects). Field defects are areas where sown plants poorly develop due to sowing failures or extreme local conditions (soil humidity, missing nutrients). In twenty oilseed rape fields, we studied carabid assemblages collected with pitfall traps in three habitat types (field interiors, field defects, and boundaries between them) and in two sampling periods (spring and summer). Both activity-density and species richness were lower in field defects than in boundaries and field interiors during both sampling periods, indicating that field defects were not a preferred habitat for carabids. Activity-density and species richness significantly increased from spring to summer in all habitat types. Species composition of carabid assemblages significantly differed between field defects and field interiors or boundaries. Field defects were characterised by impoverished carabid assemblages and the presence of few indicator species. Interestingly, field defects with well-developed plant cover hosted carabid assemblages with species richness comparable to field interiors, indicating that re-sowing of field defects can support carabid populations within arable fields. However, the consequences of re-sowing on other arthropod taxa, e.g., insects requiring habitats with bare ground, and on populations of rare weeds need to be evaluated. The lack of effects of field defect size on carabid assemblages indicated that carabid beetles react to even very small patches with unsuitable conditions (e.g., very low humidity, high temperature or food scarcity).
1. Introduction The global human population has increased considerably over the last decades and keeps growing at a rate that requires a more than twofold increase in agricultural production in the next 30 years in order to fulfil global food demands (Tilman et al., 2001). To achieve this goal, agricultural intensification, through several changes at local and landscape scales, has been the main approach to increase yields in Europe and the rest of the world (Emmerson et al., 2016). These changes include increasing external inputs and mechanization of agricultural practices, decreasing crop diversity by growing a reduced number of species in larger fields, and the destruction and fragmentation of natural habitats (Tscharntke et al., 2005). As a result, agroecosystems have become dominant, covering 40 % of the Earth’s land surface (Foley
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et al., 2005). This has negative effects on biodiversity (Benton et al., 2003; Firbank et al., 2008), soil quality (Cassman, 1999), and ecosystem services (Tscharntke et al., 2005). Landscape heterogeneity, including both the diversity of different habitats and their configuration, is a well-known driver of biodiversity in agroecosystems (Fahrig et al., 2011). Natural and semi-natural permanent non-crop habitats, such as woodlots (Gonzalez et al., 2015; Knapp and Rezac, 2015), hedgerows, and field margins (Varchola and Dunn, 2001; Pollard and Holland, 2006; Lovei and Magura, 2017) enrich arthropod communities in agroecosystems. Agri-environmental schemes (AES) that promote the creation of non-crop habitats, such as grassy strips, are also beneficial for many arthropod species inhabiting agroecosystems (Kleijn et al., 2006; Batary et al., 2011; Gayer et al., 2019). Habitats created within the AES framework can contribute to
Corresponding author. E-mail address: [email protected] (M. Knapp).
https://doi.org/10.1016/j.agee.2020.106856 Received 15 November 2019; Received in revised form 29 January 2020; Accepted 3 February 2020 0167-8809/ © 2020 Published by Elsevier B.V.
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(Boetzl et al., 2019). The highest species richness is commonly recorded at boundaries between neighbouring habitat types, i.e., strong edge effects are observed in carabids (Magura et al., 2017; Fusser et al., 2018; Knapp et al., 2019; Pardon et al., 2019). Species composition of carabid assemblages inhabiting non-crop habitats is also strongly affected by local vegetation characteristics (Brose, 2003a; Harvey et al., 2008; Pakeman and Stockan, 2014). Even very small non-crop habitats with specific environmental conditions can host species missing from field interiors, i.e., areas planted with crop (Brose, 2003c; Knapp and Rezac, 2015). The main aim of this study was to investigate the spatial distribution of carabid beetles within oilseed rape (OSR) fields with field defects. Data were collected in three habitat types within OSR fields – the field interior, on the boundary between field defect and crop, and in field defect patches. We also investigated temporal variation in carabid assemblages, comparing spring (flowering) and summer (crop maturing) periods. We expected field defects within OSR fields to have distinct environmental characteristics, in contrast to the surrounding crop monoculture. Thus, we predicted that the composition of carabid assemblages in field defects would differ from the surrounding habitats and contribute to increased field-level biodiversity. Moreover, we hypothesized that boundaries between field defects and OSR crop could be colonised by species from both habitats and thus will host the most diverse carabid assemblages. We also expected that the carabid assemblages in field defects would be affected by the defect features, such as size and degree of plant cover. Specifically, we predicted that carabids would benefit from high level plant cover as it positively modify microclimate, improve food availability (plants host herbivores that can be eaten by carabids), and provide shelter for carabids against their predators (both vertebrates and arthropods).
maintaining larger populations of dispersal-limited predatory species and can act as source habitats for beneficial natural enemies that spill over into arable fields (Tschumi et al., 2016; Boetzl et al., 2019). The spillover effects can be especially in spring when adults that overwintered in non-crop habitats recolonise adjacent arable fields (Geiger et al., 2009; Blitzer et al., 2012). Non-crop habitats sustain field-inhabiting species when some resources are temporarily missing within arable fields, e.g., after large-scale disturbances like harvest or tillage (Rand et al., 2006; Blitzer et al., 2012). Therefore, agricultural landscapes containing permanent non-crop habitats can support higher levels of ecosystem services such as pest suppression (Bianchi et al., 2006), weed suppression (Bohan et al., 2011), and pollination (Garibaldi et al., 2011). However, while the positive effects of permanent non-crop habitats are well established, studies investigating the influence of transient spontaneous non-crop patches within arable fields are rare. To our knowledge, the existing research on terrestrial insect assemblages in transient habitats within arable fields is restricted to the study of temporarily waterlogged areas (Brose, 2003a, b, c) or artificially created islands in arable fields (‘beetle banks’) that would act in a similar way in the first season (Thomas et al., 1991). Here, we investigated the biodiversity contribution of field defects, spontaneously occurring temporary non-crop habitats within arable fields. Crop fields are not completely homogeneous, even if machine-sowing should generate a uniform crop stand. Crop seed may fail to germinate, extreme conditions (e.g., very low soil humidity) can kill the crop, or it can grow extremely sparsely or slowly due to a local lack of nutrients. Field defects can also arise due to sowing failure caused by machine itself or its operator. Such habitat islands are typically dry, in contrast to temporarily waterlogged areas, with a low vegetation cover and a high proportion of bare ground compared to the surrounding crop cover. Field defects can be large and common, especially in years with extreme weather conditions (e.g., very low precipitation; Fig. 1) or when the crop vegetation is damaged by pests, including vertebrates. Despite being often locally abundant, the importance of field defects for beneficial arthropods is largely unknown. Carabid beetles are abundant natural enemies of pests and weed seeds in arable fields, thus playing important role in agroecosystems (Lovei and Sunderland, 1996; Bohan et al., 2011; Dainese et al., 2017). Carabid assemblages can be affected by both landscape characteristics, e.g., the distance to nearest non-crop habitats or habitat island size, and local habitat characteristics, e.g., the structure of vegetation cover (Brose, 2003a; Knapp and Rezac, 2015; Djoudi et al., 2019; Knapp et al., 2019). The number of carabid species commonly decreases from field edges adjacent to non-crop habitats to field interiors (Saska et al., 2007; Knapp et al., 2019), which confirms the importance of landscape heterogeneity for ecosystem services provision within arable fields
2. Materials and methods 2.1. Sampling sites Carabid beetles (Coleoptera: Carabidae) were sampled within 20 arable fields located in the north-western part of the Czech Republic (Fig. 2a; for GPS coordinates see Appendix A1). Only winter oilseed rape fields with field defects were selected for our study. Field defects are temporary patches where sown plants are poorly developed and other plant species can emerge (Fig. 2b; Appendix A2). In our study area, field defects are quite common phenomenon and defects can reach relatively large size in fields prone to their emergence. The size of field defects investigated in this study ranged from 10 to 66 m in diameter (for details see Appendix A1). Field interiors were defined as parts of the crop field with well-developed oilseed rape plants, separated from field edges and defects by at least 15 m to avoid edge effects.
Fig. 1. Aerial images showing examples of field defects from Czech Republic. Large field defect covering several hectares (a); re-sown field defect (b); small field defect of just few tens of square metres. Aerial images were obtained from the server www.mapy.cz (accessed on 27 October 2019). 2
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Fig. 2. Study area. Map showing distribution of 20 oilseed rape fields (nine north of Labe river and eleven south of Labe river) with field defects investigated in our study (a). A photography of one of investigated field defects (b).
samples collected by particular undamaged / undestroyed pitfall traps. The effects of habitat type (crop interior, boundary, and field defect) and sampling period (spring, summer) on carabid beetle activity-density and species richness were analyzed using Generalized Linear Mixed Models (GLMMs). For species richness, the Poisson error distribution with a log link was used. Activity-density data showed overdispersion and therefore a negative binomial error distribution was used instead. The field as well as habitat type nested within field were used as random effects in our models to account for the nested design of the study. The independent variables were habitat type, sampling period, and the interaction between habitat type and sampling period. For model selection, we started with the full model and simplified it according to Likelihood Ratio Tests by removing non-significant variables (α = 0.05). All analyses were performed with the software R (R Development Core Team, 2017), package lme4 (Bates et al., 2015). Differences in the species composition of carabid beetle assemblages between habitats and sampling periods were analysed using NMDS (Non-metric multidimensional scaling analysis) and Permanova (Permutational multivariate analysis of variance) multivariate analyses based on the Bray-Curtis index of dissimilarity between samples, calculated with log-transformed species abundance data (log N + 1). NMDS provides a visual representation of the dissimilarity in carabid beetle species composition between samples (Shepard, 1962), whereas Permanova uses permutations of the data to provide significance tests for the independent variables (Anderson, 2001), habitat type and sampling period in our case. Furthermore, in order to test if carabid assemblages in field defects and boundaries represented a distinct set of species or a subset of the species present in OSR crop, we calculated the matrix temperature. This metric measures the degree of nestedness on species per sites matrices and values can range from 0 to 100°, with low temperatures indicating higher degrees of nestedness and high temperatures random distributions of species among sites (Atmar and Patterson, 1993). We calculated matrix temperature separately for each of the 20 fields to measure local nestedness among habitats. These analyses were performed in R with the package vegan (Oksanen et al., 2007). Finally, we performed an Indicator Species analysis with the R package indicspecies (De Caceres and Legendre, 2009) to determine if there were ground beetle species closely linked to field defects, OSR fields, or boundaries between the two. To analyse the effects of field defect characteristics on carabid assemblages, we calculated the difference in activity-density and species richness between field defects and field interiors. We used mean activity-density of the three traps per habitat and the accumulated species richness to calculate these variables. Differences in activity-density and species richness between field defects and field interiors were used as response variables in LMMs with a normal distribution, and field as a
2.2. Data collection To investigate the effects of field defects on activity-density (number of collected individuals), species richness and species composition, carabid beetles were sampled using pitfall traps. Carabid beetles were collected in two sampling periods (each 21 days long) from late May to June 11 and from June 12 to early July. The timing was selected to cover different phenological phases of the crop (flowering vs. seed maturation). In total, 180 pitfall traps were operated during each sampling period. Pitfall traps were made of 400 ml plastic cups, dug into the soil with the rim of the cup flush with the soil surface (9.5 cm in diameter). All cups were filled with 200 ml of propylene glycolwater solution (1:3, v/v) as a killing and preservative fluid. This fluid is efficient for collecting carabid beetles and is relatively non-toxic to nontarget organisms (Knapp and Ruzicka, 2012). Pitfall traps were covered by roofs made of an aluminium sheet (25 × 35 cm) to prevent flooding during heavy rainfall and to protect the traps from damage by large mammals (e.g., wild boars and roe deer). Roofs were placed 5 cm above the openings of the cups using three long nails. Shallow ditches were dug around traps along the slope to prevent flooding from water flowing over the surface. A set of three pitfall traps arranged 5 m apart were installed in three habitats per field: 1) field defect (central part); 2) boundary between the crop and field defect; 3) field interior (area with well-developed OSR plants). In total, nine pitfall traps were exposed per field in each period. Fifteen traps out of 360 were damaged or destroyed by wild boars and foxes. Samples originating from damaged or destroyed traps were omitted from our analyses. In all cases at least one trap out of three installed per habitat type remained undamaged. After sample collection, surplus preservation fluid was removed by sieving in the field and pitfall trap samples were transported to the laboratory. Pitfall samples were placed individually into plastic bags, and were coded and stored in at −20 °C until processing. Later, all carabid beetles were extracted from the pitfall samples and identified to species using the identification guide by Hůrka (1996). In early May, field defects were almost without any vegetation (weed cover) but some of them started to become overgrown during the following weeks. We measured the vegetation cover of each field defect between the first and second sampling period using a visual estimation of the proportion of bare ground and vegetation cover. In order to reduce sampling bias, the same observers (MS and MK) performed these estimations. At the same time, the size (diameter) of each field defect was directly measured using a tape measure. 2.3. Statistical analyses Statistical analyses are based on 345 data points representing 3
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defects (Fig. 3a; Tukey´s t-tests p < 0.001 for boundaries and field interiors). More carabid species were recorded in the summer than in the spring period (mean 5.6 ± 0.2 in spring vs. 8.0 ± 0.2 in summer; Fig. 3a), which corresponded well to the pattern observed for activitydensity. The interaction between habitat type and sampling period was not significant (GLMM: χ22,337 = 2.64; p = 0.27).
random variable. Independent variables were field defect size (logarithm of the diameter), proportion of vegetation cover, sampling period and the paired interactions between these variables. Model selection was performed as explained above. The analyses were performed using the R package nlme (Pinheiro et al., 2013). 3. Results
3.3. Species composition In total, 27 076 carabid beetles of 75 species were collected (Appendix A3). We registered a shift in the dominant species across the habitat types. The three most common species in field defects were Poecilus cupreus (2467 individuals), Brachinus crepitans (1136 individuals) and Pterostichus melanarius (943 individuals), whereas the most common species in boundaries were Poecilus cupreus (2754 individuals), Brachinus crepitans (1572 individuals) and Anchomenus dorsalis (1458 individuals), and in field interiors the most common species were Anchomenus dorsalis (2583 individuals), Poecilus cupreus (2143 individuals) and Amara ovata (2076 individuals). This clearly indicated that some abundant species were avoiding field defects, e.g., Anchomenus dorsalis and Amara ovata, whereas other kept their activitydensity in field defects comparable to surrounding OSR crop, e.g., Poecilus cupreus, or even increased their activity-density in field defects and defect boundaries, e.g., Harpalus signaticornis (Appendix A3).
Multivariate analyses of species composition showed differences between habitat types and sampling periods (Fig. 4). The Permanova indicated significant effects of habitat type (F1,337 = 20.00; p = 0.001; R2 = 0.10), sampling period (F1,337 = 25.15; p = 0.001; R2 = 0.06), and their interaction (F1,337 = 3.53; p = 0.001; R2 = 0.02) on carabid species composition. The NMDS bi-plot indicate a significant gradient from field defect samples to field interiors in the first NMDS axis (Fig. 4). The difference in species composition between field defects and other habitat types was caused mainly by reduced numbers of several abundant species in field defects, e.g., Amara ovata, Amara similata, Anchomenus dorsalis and Brachinus explodens (Appendix A3). The nestedness analysis resulted in low mean matrix temperature per field (only 3.81° ± 0.37), indicating a high degree of nestedness among habitats. Indicator Species analysis confirmed that only Bembidion quadrimaculatum was associated with field defects, Bembidion lampros and Microlestes minutulus were linked to field defects and boundaries, and the four abundant species mentioned above (Anchomenus dorsalis, Amara ovata, Amara similata, and Brachinus explodens) were associated with boundaries and OSR crops (Appendix A4).
3.1. Activity-density Total carabid activity-density was significantly influenced by habitat type (GLMM: χ22,336 = 21.87; p < 0.001), sampling period (GLMM: χ21,336 = 178.12; p < 0.001), and the interaction between habitat type and sampling period (GLMM: χ22,336 = 15.14; p < 0.001; Fig. 3b). In spring, activity-density was significantly lower in field defects than in field interiors (Tukey´s t test, p = 0.002) or boundaries (Tukey´s t test, p = 0.005), whereas no differences between field interiors and boundaries were found (Tukey´s t test, p = 0.97). In summer, activity-density increased in all three habitat types (mean 43.7 ± 4.8 in spring vs. 113.9 ± 8.5 in summer). Similarly to spring, activity-density was lowest in field defects (Tukey´s t-tests, p < 0.001 for both boundaries and field interiors). However, there was also a tendency for marginally higher activity-density in field interiors compared to boundaries (Tukey´s t test, p = 0.06).
3.4. Effects of field defect characteristics The difference in carabid activity-density between field defects and crop interiors was affected by the sampling period (LME: F1,37 = 13.06; p = 0.002). The difference was higher in summer due to the relatively higher activity-densities in crop interiors at this time (see Section 3.1). There were no significant effects of field defect size, vegetation cover, and interactions between sampling period and defect size or vegetation cover on the difference in carabid activity-density between field defects and crop interiors (Appendix A5). This indicates that even very small field defects reduced carabid activity-density in their central parts. The difference in carabid beetle richness between field defects and crop interiors decreased significantly with the increasing proportion of vegetation cover in field defects (LME: F1,37 = 7.92; p = 0.012; Fig. 5). Note that field defects with more than 80 % of vegetation cover hosted similar numbers of carabid species as OSR field interiors. Field defect size, sampling period, and the interaction between these variables were not important for the difference in carabid species richness between
3.2. Species richness Carabid species richness was affected by habitat type (GLMM: χ22,339 = 22.91; p < 0.001) and sampling period (GLMM: χ21,339 = 71.87; p < 0.001). Species richness was similar in field interiors and habitat boundaries (Tukey´s t-test p = 0.83), but significantly lower in field
Fig. 3. Effects of habitat type and sampling period on (a) species richness and (b) activity-density of carabid beetle assemblages in oilseed rape fields. Predictions of the best GLMMs (mean ± 95 % confidence intervals) are shown. 4
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Fig. 4. Effects of habitat type on species composition of carabid beetle assemblages. Non-metric multidimensional scaling ordination diagram based on species abundances (log-transformed) is shown. Habitat types represented are: field defects (D; red), boundaries (B; black), and oilseed rape field interiors (F; green). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
second (summer) period. The bare ground was directly exposed to sunshine and local temperatures within field defects were thus much higher than in OSR field interiors (Appendix A6). Many carabid species cannot tolerate even short-term exposure to temperatures over 50 °C (Thiele, 1977; Slatyer and Schoville, 2016). Vegetation-free soil also dries out faster, and water availability seems to be a limiting factor for carabids (Thiele, 1977; Holland, 2002). Water availability is also crucial for plant growth, thereby slowing down the development of vegetation within field defects during summer. Low abundance of plants has a direct negative effect on abundance of herbivores and detritivores, and thus reduces potential food sources for carabids (Cameron and Leather, 2012). Field defects thus look like low productivity islands within arable fields. Several studies focused on carabid beetle assemblages inhabiting non-crop habitats within arable fields show that carabid activity-density and species richness can be positively related to habitat productivity (Eyre et al., 2013; Knapp and Rezac, 2015). Bare soil could also increase the predation risk experienced by carabid beetles themselves (Blubaugh et al., 2017). Vertebrate predators as well as arthropod intra-guild competitors of carabid beetles, e.g., spiders and ants, can be more effective in vegetation-free field defects than in field defects with dense vegetation (Lovei and Sunderland, 1996). On the other hand, field defect boundaries are a quite attractive habitat to many carabid species. For several species the highest activitydensity was recorded at boundaries (Appendix A3) and overall carabid species richness peaked at boundaries between field defects and field interiors. This finding is in line with studies that recorded positive edge effects on carabid assemblages observed at boundaries between arable fields and neighbouring permanent non-crop habitats (Magura et al., 2017; Knapp et al., 2019). Both spillover between neighbouring habitats and existence of edge specialist species can be responsible for the observed pattern (Knapp et al., 2019).
Fig. 5. Effects of plant cover within field defects on the difference in species richness of carabid beetles between field defects and field interiors. The slope (black line) and 95 % confidence interval (grey band) estimated from the best LMM are shown.
field defects and crop interiors (Appendix A5). 4. Discussion 4.1. Summary of main results In general, field defects seem to be suboptimal habitats for carabid beetles inhabiting Central European OSR fields. Contrary to our prediction that field defects within OSR fields will significantly enhance local activity-density and diversity of carabids via increased habitat heterogeneity, both activity-density and species richness were higher within OSR crop interiors compared to field defects. We recorded higher activity-density and species richness in the summer period compared to spring. Carabid activity-density tended to be highest within OSR crop interiors, whereas carabid species richness tended to peak on the boundary between OSR crop and field defect. Only a few carabid species occurred more frequently in field defects than in the surrounding crop. Our results also indicate that the spatial distribution of carabid beetles within OSR crops with field defects varied over time.
4.3. Do field defects represent unique and valuable habitats for carabids? Landscape heterogeneity and the presence of non-crop habitats in agroecosystems is one of the most important factors affecting local biodiversity and provision of ecological services (Bianchi et al., 2006; Gonzalez et al., 2017). Even species-poor habitats hosting unique species can increase species richness at the landscape level (Knapp and Rezac, 2015). Our results suggest that carabid diversity can be slightly enhanced at boundaries between OSR crops and field defects. However, carabid assemblages in field defects did not differ from boundary and field interior assemblages by the presence of many unique species, but rather the activity-density of several dominant species was reduced
4.2. Field defect effects on activity-density and species richness Factors affecting the presence of carabid beetles in field defects are probably related to abiotic characteristics of this specific habitat. The investigated field defects were predominantly covered by bare ground in the first (spring) sampling period and some of them even in the 5
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Funding
there. Three small carabid species Bembidion quadrimaculatum, Bembidion lampros and Microlestes minutulus were identified as the indicator species typical for field defects; indeed, these species were quite rare in our study system (only 20, 131 and 18 individuals were collected, respectively). Thus, contrary to our expectations, field defects hosted mainly impoverished carabid assemblages from the OSR crop with very few species unique to field defects. This conclusion is also supported by a very high nestedness of carabid assemblages within arable fields investigated in our study.
This study was supported by the Internal Grant Agency of Faculty of Environmental Sciences, Czech University of Life Sciences Prague (grant number 42110/1312/3118) and the Czech Science Foundation (grant number 18-26542S). Declaration of Competing Interest None.
4.4. How to improve field defects
Acknowledgments
Field defects with a high weed cover hosted carabid assemblages with their species richness comparable to those in OSR crop interiors, but field defects with a high proportion of bare ground hosted speciespoor carabid assemblages. This fact supports the idea of vegetating large field defects, a practice already followed by some Czech farms (Fig. 1b). Planting nectar-rich plant communities there would also be beneficial to pollinators and other insects. Support of such activities by an agri-environmental scheme (AES) could be a possibility. On the other hand, bare ground can be more than 10 °C warmer compared to field interiors (Balisky and Burton, 1995), also supported by our measurements; see Appendix A6), which is detrimental in peaking summer, but can be beneficial for ectothermic animals in early spring and on cold days (Key, 2000). Moreover, bare soil can also be a suitable habitat for some solitary bees and wasps for nesting, and a good hunting place for other beneficial insects (Fry and Lonsdale, 1991). However, nearby vegetation seems to be necessary (Mazia et al., 2006; Cameron and Leather, 2012) and thus small areas of bare ground in defects predominantly covered by vegetation might be ideal. Especially in the case of large field defects, Czech farmers sometimes re-sow field defects with other crops that improve soil quality, e.g., legumes. This indicates that re-sowing practice can be quite easily adopted by farmers even without subsidies (specific AES; see Fig. 1b). However, future studies are needed to compare biodiversity of bare and re-sown field defects across multiple taxa to determine if re-sowing is the best management strategy in all cases. Considering the relevance of bare ground for some insects (Key, 2000), the combination of re-sowing most of the area and leaving strips of bare ground around could be most suitable solution for enhancing biodiversity within field defects. Note also that field defects with naturally developed weedy vegetation can host rare and threatened plant species (Appendix A2) and also bird populations are enhanced in similar habitats called “lark windows” in Germany (Oberwelland and Nottmeyer-Linden, 2009). Therefore, we predict that re-sowing all field defects can be used only in specific cases and at least some field defects should remain without any intervention.
We would like to thank the owners of the fields for their permission to perform fieldwork, Jana Zemanová for her help in field, Martin Štrobl for his help in laboratory, Tiit Teder for helpful comments on the previous version of our manuscript and Mark Francis Sixsmith for language corrections. We are grateful to three anonymous reviewers for their insightful and constructive suggestions that helped to improve our manuscript. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2020.106856. References Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26, 32–46. Atmar, W., Patterson, B.D., 1993. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382. Balisky, A.C., Burton, P.J., 1995. Root-zone soil-temperature variation associated with microsite characteristics in high-elevation forest openings in the interior of BritishColumbia. Agric. For. Meteorol. 77, 31–54. Batary, P., Baldi, A., Kleijn, D., Tscharntke, T., 2011. Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc. R. Soc. B-Biol. Sci. 278, 1894–1902. Bates, D., Machler, M., Bolker, B.M., Walker, S.C., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188. Bianchi, F.J.J.A., Booij, C.J.H., Tscharntke, T., 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B 273, 1715–1727. Blitzer, E.J., Dormann, C.F., Holzschuh, A., Klein, A.-M., Rand, T.A., Tscharntke, T., 2012. Spillover of functionally important organisms between managed and natural habitats. Agric. Ecosyst. Environ. 146, 34–43. Blubaugh, C.K., Widick, I.V., Kaplan, I., 2017. Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels. Oecologia 185, 1–11. Boetzl, F.A., Krimmer, E., Krauss, J., Steffan-Dewenter, I., 2019. Agri-environmental schemes promote ground-dwelling predators in adjacent oilseed rape fields: Diversity, species traits and distance-decay functions. J. Appl. Ecol. 56, 10–20. Bohan, D.A., Boursault, A., Brooks, D.R., Petit, S., 2011. National-scale regulation of the weed seedbank by carabid predators. J. Appl. Ecol. 48, 888–898. Brose, U., 2003a. Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135, 407–413. Brose, U., 2003b. Island biogeography of temporary wetland carabid beetle communities. J. Biogeogr. 30, 879–888. Brose, U., 2003c. Regional diversity of temporary wetland carabid beetle communities: a matter of landscape features or cultivation intensity? Agric. Ecosyst. Environ. 98, 163–167. Cameron, K.H., Leather, S.R., 2012. Heathland management effects on carabid beetle communities: the relationship between bare ground patch size and carabid biodiversity. J. Insect Conserv. 16, 523–535. Cassman, K.G., 1999. Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. PNAS 96, 5952–5959. Dainese, M., Schneider, G., Krauss, J., Steffan-Dewenter, I., 2017. Complementarity among natural enemies enhances pest suppression. Sci. Rep. 7, 8172. De Caceres, M., Legendre, P., 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90, 3566–3574. Djoudi, E., Plantegenest, M., Aviron, S., Petillon, J., 2019. Local vs. landscape characteristics differentially shape emerging and circulating assemblages of carabid beetles in agroecosystems. Agric. Ecosyst. Environ. 270, 149–158. Emmerson, M., Morales, M.B., Onate, J.J., Batry, P., Berendse, F., Liira, J., Aavik, T., Guerrero, I., Bommarco, R., Eggers, S., Part, T., Tscharntke, T., Weisser, W., Clement,
5. Conclusion Natural field defects within OSR fields hosted less species-rich carabid assemblages compared to assemblages in OSR crop and boundaries. Moreover, the activity-density of several dominant carabid species was strongly reduced in field defects and only a few carabid species were more abundant there. Thus, the avoidance of even very small field defects confirms the ability of carabid species to be used as bioindicators of habitat quality, even at very small scales (Brose, 2003a, c; Rainio and Niemela, 2003; Knapp and Rezac, 2015). Importantly, the positive influence of vegetation cover on carabid richness in field defects indicates that re-sowing field defects or supporting natural weed communities can be a useful habitat management measure to support carabids within arable fields. However, future research is needed to determine if field defects support other groups of beneficial or endangered arthropods and to confirm whether re-sowing will also improve field defect quality for them. 6
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Rep. 9, 8967. Lovei, G.L., Magura, T., 2017. Ground beetle (Coleoptera: Carabidae) diversity is higher in narrow hedges composed of a native compared to non-native trees in a Danish agricultural landscape. Insect Conserv. Divers. 10, 141–150. Lovei, G.L., Sunderland, K.D., 1996. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu. Rev. Entomol. 41, 231–256. Magura, T., Lovei, G.L., Tothmeresz, B., 2017. Edge responses are different in edges under natural versus anthropogenic influence: a meta-analysis using ground beetles. Ecol. Evol. 7, 1009–1017. Mazia, C.N., Chaneton, E.J., Kitzberger, T., 2006. Small-scale habitat use and assemblage structure of ground-dwelling beetles in a Patagonian shrub steppe. J. Arid Environ. 67, 177–194. Oberwelland, C., Nottmeyer-Linden, K., 2009. Praktische Schutzmaßnahmen für Feldvögel. Nat. NRW 3, 31–33. Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, H.M.H., 2007. The vegan package. Community Ecol. Package 10, 631–637. Pakeman, R.J., Stockan, J.A., 2014. Drivers of carabid functional diversity: abiotic environment, plant functional traits, or plant functional diversity? Ecology 95, 1213–1224. Pardon, P., Reheul, D., Mertens, J., Reubens, B., De Frenne, P., De Smedt, P., Proesmans, W., Van Vooren, L., Verheyen, K., 2019. Gradients in abundance and diversity of ground dwelling arthropods as a function of distance to tree rows in temperate arable agroforestry systems. Agric. Ecosyst. Environ. 270, 114–128. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Development Core Team, R., 2013. Nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3. pp. 1–107. Pollard, K.A., Holland, J.M., 2006. Arthropods within the woody element of hedgerows and their distribution pattern. Agric. For. Entomol. 8, 203–211. R Development Core Team, 2017. A Language and Environment for Statistical Computing. Available at. http://www.R-project.org. Rainio, J., Niemela, J., 2003. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers. Conserv. 12, 487–506. Rand, T.A., Tylianakis, J.M., Tscharntke, T., 2006. Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol. Lett. 9, 603–614. Saska, P., Vodde, M., Heijerman, T., Westerman, P., van der Werf, W., 2007. The significance of a grassy field boundary for the spatial distribution of carabids within two cereal fields. Agric. Ecosyst. Environ. 122, 427–434. Shepard, R.N., 1962. The analysis of proximities: multidimensional scaling with an unknown distance function. Psychometrika 27, 125–140. Slatyer, R.A., Schoville, S.D., 2016. Physiological limits along an elevational gradient in a radiation of montane ground beetles. PLoS One 11, e0151959. Thiele, T.U., 1977. Carabid Beetles in Their Environments: a Study on Habitat Selection by Adaptations in Physiology and Behaviour. Springer-Verlag. Thomas, M.B., Wratten, S.D., Sotherton, N.W., 1991. Creation of island habitats in farmland to manipulate populations of beneficial arthropods – predator densities and emigration. J. Appl. Ecol. 28, 906–917. Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001. Forecasting agriculturally driven global environmental change. Science 292, 281–284. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol. Lett. 8, 857–874. Tschumi, M., Albrecht, M., Collatz, J., Dubsky, V., Entling, M.H., Najar-Rodriguez, A.J., Jacot, K., 2016. Tailored flower strips promote natural enemy biodiversity and pest control in potato crops. J. Appl. Ecol. 53, 1169–1176. Varchola, J.M., Dunn, J.P., 2001. Influence of hedgerow and grassy field borders on ground beetle (Coleoptera: Carabidae) activity in fields of corn. Agric. Ecosyst. Environ. 83, 153–163.
L., Bengtsson, J., 2016. How agricultural intensification affects biodiversity and ecosystem services. In: Dumbrell, A.J., Kordas, R.L., Woodward, G. (Eds.), Advances in Ecological Research, Vol 55: Large-Scale Ecology: Model Systems to Global Perspectives, pp. 43–97. Eyre, M.D., Luff, M.L., Leifert, C., 2013. Crop, field boundary, productivity and disturbance influences on ground beetles (Coleoptera, Carabidae) in the agroecosystem. Agric. Ecosyst. Environ. 165, 60–67. Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C., Siriwardena, G.M., Martin, J.L., 2011. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol. Lett. 14, 101–112. Firbank, L.G., Petit, S., Smart, S., Blain, A., Fuller, R.J., 2008. Assessing the impacts of agricultural intensification on biodiversity: a British perspective. Phil. Trans. R. Soc. B 363, 777–787. Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574. Fry, R., Lonsdale, D., 1991. Habitat Conservation for Insects: a Neglected Green Issue. Amateur Entomologists’ Society. Fusser, M.S., Holland, J.M., Jeanneret, P., Pfister, S.C., Entling, M.H., Schirmel, J., 2018. Interactive effects of local and landscape factors on farmland carabids. Agric. For. Entomol. 20, 549–557. Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhoffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyorgyi, H., Viana, B.F., Westphal, C., Winfree, R., Klein, A.M., 2011. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 14, 1062–1072. Gayer, C., Lovei, G.L., Magura, T., Dieterich, M., Batary, P., 2019. Carabid functional diversity is enhanced by conventional flowering fields, organic winter cereals and edge habitats. Agric. Ecosyst. Environ. 284, 106579. Geiger, F., Wackers, F., Bianchi, F., 2009. Hibernation of predatory arthropods in seminatural habitats. Biocontrol 54, 529–535. Gonzalez, E., Salvo, A., Valladares, G., 2015. Sharing enemies: evidence of forest contribution to natural enemy communities in crops, at different spatial scales. Insect Conserv. Divers. 8, 359–366. Gonzalez, E., Salvo, A., Valladares, G., 2017. Arthropod communities and biological control in soybean fields: forest cover at landscape scale is more influential than forest proximity. Agric. Ecosyst. Environ. 239, 359–367. Harvey, J.A., van der Putten, W.H., Turin, H., Wagenaar, R., Bezemer, T.M., 2008. Effects of changes in plant species richness and community traits on carabid assemblages and feeding guilds. Agric. Ecosyst. Environ. 127, 100–106. Holland, J.M., 2002. The Agroecology of Carabid Beetles. Intercept, Andover, UK. Hůrka, K., 1996. Carabidae of the Czech and Slovak Republics. Carabidae České a Slovenské republiky, Kabourek, Zlín. Key, R., 2000. Bare ground and the conservation of invertebrates. Br. Wildl. 2, 183–191. Kleijn, D., Baquero, R.A., Clough, Y., Diaz, M., De Esteban, J., Fernandez, F., Gabriel, D., Herzog, F., Holzschuh, A., Johl, R., Knop, E., Kruess, A., Marshall, E.J.P., SteffanDewenter, I., Tscharntke, T., Verhulst, J., West, T.M., Yela, J.L., 2006. Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol. Lett. 9, 243–254. Knapp, M., Rezac, M., 2015. Even the smallest non-crop habitat islands could be beneficial: distribution of carabid beetles and spiders in agricultural landscape. PLoS One 10, e0123052. Knapp, M., Ruzicka, J., 2012. The effect of pitfall trap construction and preservative on catch size, species richness and species composition of ground beetles (Coleoptera: Carabidae). Eur. J. Entomol. 109, 419–426. Knapp, M., Seidl, M., Knappova, J., Macek, M., Saska, P., 2019. Temporal changes in the spatial distribution of carabid beetles around arable field-woodlot boundaries. Sci.
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Temporary non-crop habitats within arable fields: The effects of field defects on carabid beetle assemblages
T
Miroslav Seidla, Ezequiel Gonzáleza, Tomáš Kadleca, Pavel Saskaa,b, Michal Knappa,* a b
Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Prague - Suchdol, 165 00, Czech Republic Crop Research Institute, Drnovská 507, Prague 6 - Ruzyně, 161 06, Czech Republic
A R T I C LE I N FO
A B S T R A C T
Keywords: Agri-environmental schemes Agricultural landscape Biodiversity Carabidae Ecosystem services Ephemeral habitats Oilseed rape
Landscape heterogeneity and higher complexity generally increase biodiversity in agroecosystems. Carabid beetles represent abundant and important predators of pests and weed seeds in temperate agroecosystems and are affected by landscape structure. Several studies have described the impact of permanent non-crop habitats such as woodlots, hedgerows, and grassy margins on carabid assemblages. However, temporal non-crop habitat islands within arable fields have been rarely investigated. The aim of this study was to investigate spatial distribution of carabid beetles within oilseed rape fields having temporary non-crop habitats (field defects). Field defects are areas where sown plants poorly develop due to sowing failures or extreme local conditions (soil humidity, missing nutrients). In twenty oilseed rape fields, we studied carabid assemblages collected with pitfall traps in three habitat types (field interiors, field defects, and boundaries between them) and in two sampling periods (spring and summer). Both activity-density and species richness were lower in field defects than in boundaries and field interiors during both sampling periods, indicating that field defects were not a preferred habitat for carabids. Activity-density and species richness significantly increased from spring to summer in all habitat types. Species composition of carabid assemblages significantly differed between field defects and field interiors or boundaries. Field defects were characterised by impoverished carabid assemblages and the presence of few indicator species. Interestingly, field defects with well-developed plant cover hosted carabid assemblages with species richness comparable to field interiors, indicating that re-sowing of field defects can support carabid populations within arable fields. However, the consequences of re-sowing on other arthropod taxa, e.g., insects requiring habitats with bare ground, and on populations of rare weeds need to be evaluated. The lack of effects of field defect size on carabid assemblages indicated that carabid beetles react to even very small patches with unsuitable conditions (e.g., very low humidity, high temperature or food scarcity).
1. Introduction The global human population has increased considerably over the last decades and keeps growing at a rate that requires a more than twofold increase in agricultural production in the next 30 years in order to fulfil global food demands (Tilman et al., 2001). To achieve this goal, agricultural intensification, through several changes at local and landscape scales, has been the main approach to increase yields in Europe and the rest of the world (Emmerson et al., 2016). These changes include increasing external inputs and mechanization of agricultural practices, decreasing crop diversity by growing a reduced number of species in larger fields, and the destruction and fragmentation of natural habitats (Tscharntke et al., 2005). As a result, agroecosystems have become dominant, covering 40 % of the Earth’s land surface (Foley
⁎
et al., 2005). This has negative effects on biodiversity (Benton et al., 2003; Firbank et al., 2008), soil quality (Cassman, 1999), and ecosystem services (Tscharntke et al., 2005). Landscape heterogeneity, including both the diversity of different habitats and their configuration, is a well-known driver of biodiversity in agroecosystems (Fahrig et al., 2011). Natural and semi-natural permanent non-crop habitats, such as woodlots (Gonzalez et al., 2015; Knapp and Rezac, 2015), hedgerows, and field margins (Varchola and Dunn, 2001; Pollard and Holland, 2006; Lovei and Magura, 2017) enrich arthropod communities in agroecosystems. Agri-environmental schemes (AES) that promote the creation of non-crop habitats, such as grassy strips, are also beneficial for many arthropod species inhabiting agroecosystems (Kleijn et al., 2006; Batary et al., 2011; Gayer et al., 2019). Habitats created within the AES framework can contribute to
Corresponding author. E-mail address: [email protected] (M. Knapp).
https://doi.org/10.1016/j.agee.2020.106856 Received 15 November 2019; Received in revised form 29 January 2020; Accepted 3 February 2020 0167-8809/ © 2020 Published by Elsevier B.V.
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(Boetzl et al., 2019). The highest species richness is commonly recorded at boundaries between neighbouring habitat types, i.e., strong edge effects are observed in carabids (Magura et al., 2017; Fusser et al., 2018; Knapp et al., 2019; Pardon et al., 2019). Species composition of carabid assemblages inhabiting non-crop habitats is also strongly affected by local vegetation characteristics (Brose, 2003a; Harvey et al., 2008; Pakeman and Stockan, 2014). Even very small non-crop habitats with specific environmental conditions can host species missing from field interiors, i.e., areas planted with crop (Brose, 2003c; Knapp and Rezac, 2015). The main aim of this study was to investigate the spatial distribution of carabid beetles within oilseed rape (OSR) fields with field defects. Data were collected in three habitat types within OSR fields – the field interior, on the boundary between field defect and crop, and in field defect patches. We also investigated temporal variation in carabid assemblages, comparing spring (flowering) and summer (crop maturing) periods. We expected field defects within OSR fields to have distinct environmental characteristics, in contrast to the surrounding crop monoculture. Thus, we predicted that the composition of carabid assemblages in field defects would differ from the surrounding habitats and contribute to increased field-level biodiversity. Moreover, we hypothesized that boundaries between field defects and OSR crop could be colonised by species from both habitats and thus will host the most diverse carabid assemblages. We also expected that the carabid assemblages in field defects would be affected by the defect features, such as size and degree of plant cover. Specifically, we predicted that carabids would benefit from high level plant cover as it positively modify microclimate, improve food availability (plants host herbivores that can be eaten by carabids), and provide shelter for carabids against their predators (both vertebrates and arthropods).
maintaining larger populations of dispersal-limited predatory species and can act as source habitats for beneficial natural enemies that spill over into arable fields (Tschumi et al., 2016; Boetzl et al., 2019). The spillover effects can be especially in spring when adults that overwintered in non-crop habitats recolonise adjacent arable fields (Geiger et al., 2009; Blitzer et al., 2012). Non-crop habitats sustain field-inhabiting species when some resources are temporarily missing within arable fields, e.g., after large-scale disturbances like harvest or tillage (Rand et al., 2006; Blitzer et al., 2012). Therefore, agricultural landscapes containing permanent non-crop habitats can support higher levels of ecosystem services such as pest suppression (Bianchi et al., 2006), weed suppression (Bohan et al., 2011), and pollination (Garibaldi et al., 2011). However, while the positive effects of permanent non-crop habitats are well established, studies investigating the influence of transient spontaneous non-crop patches within arable fields are rare. To our knowledge, the existing research on terrestrial insect assemblages in transient habitats within arable fields is restricted to the study of temporarily waterlogged areas (Brose, 2003a, b, c) or artificially created islands in arable fields (‘beetle banks’) that would act in a similar way in the first season (Thomas et al., 1991). Here, we investigated the biodiversity contribution of field defects, spontaneously occurring temporary non-crop habitats within arable fields. Crop fields are not completely homogeneous, even if machine-sowing should generate a uniform crop stand. Crop seed may fail to germinate, extreme conditions (e.g., very low soil humidity) can kill the crop, or it can grow extremely sparsely or slowly due to a local lack of nutrients. Field defects can also arise due to sowing failure caused by machine itself or its operator. Such habitat islands are typically dry, in contrast to temporarily waterlogged areas, with a low vegetation cover and a high proportion of bare ground compared to the surrounding crop cover. Field defects can be large and common, especially in years with extreme weather conditions (e.g., very low precipitation; Fig. 1) or when the crop vegetation is damaged by pests, including vertebrates. Despite being often locally abundant, the importance of field defects for beneficial arthropods is largely unknown. Carabid beetles are abundant natural enemies of pests and weed seeds in arable fields, thus playing important role in agroecosystems (Lovei and Sunderland, 1996; Bohan et al., 2011; Dainese et al., 2017). Carabid assemblages can be affected by both landscape characteristics, e.g., the distance to nearest non-crop habitats or habitat island size, and local habitat characteristics, e.g., the structure of vegetation cover (Brose, 2003a; Knapp and Rezac, 2015; Djoudi et al., 2019; Knapp et al., 2019). The number of carabid species commonly decreases from field edges adjacent to non-crop habitats to field interiors (Saska et al., 2007; Knapp et al., 2019), which confirms the importance of landscape heterogeneity for ecosystem services provision within arable fields
2. Materials and methods 2.1. Sampling sites Carabid beetles (Coleoptera: Carabidae) were sampled within 20 arable fields located in the north-western part of the Czech Republic (Fig. 2a; for GPS coordinates see Appendix A1). Only winter oilseed rape fields with field defects were selected for our study. Field defects are temporary patches where sown plants are poorly developed and other plant species can emerge (Fig. 2b; Appendix A2). In our study area, field defects are quite common phenomenon and defects can reach relatively large size in fields prone to their emergence. The size of field defects investigated in this study ranged from 10 to 66 m in diameter (for details see Appendix A1). Field interiors were defined as parts of the crop field with well-developed oilseed rape plants, separated from field edges and defects by at least 15 m to avoid edge effects.
Fig. 1. Aerial images showing examples of field defects from Czech Republic. Large field defect covering several hectares (a); re-sown field defect (b); small field defect of just few tens of square metres. Aerial images were obtained from the server www.mapy.cz (accessed on 27 October 2019). 2
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Fig. 2. Study area. Map showing distribution of 20 oilseed rape fields (nine north of Labe river and eleven south of Labe river) with field defects investigated in our study (a). A photography of one of investigated field defects (b).
samples collected by particular undamaged / undestroyed pitfall traps. The effects of habitat type (crop interior, boundary, and field defect) and sampling period (spring, summer) on carabid beetle activity-density and species richness were analyzed using Generalized Linear Mixed Models (GLMMs). For species richness, the Poisson error distribution with a log link was used. Activity-density data showed overdispersion and therefore a negative binomial error distribution was used instead. The field as well as habitat type nested within field were used as random effects in our models to account for the nested design of the study. The independent variables were habitat type, sampling period, and the interaction between habitat type and sampling period. For model selection, we started with the full model and simplified it according to Likelihood Ratio Tests by removing non-significant variables (α = 0.05). All analyses were performed with the software R (R Development Core Team, 2017), package lme4 (Bates et al., 2015). Differences in the species composition of carabid beetle assemblages between habitats and sampling periods were analysed using NMDS (Non-metric multidimensional scaling analysis) and Permanova (Permutational multivariate analysis of variance) multivariate analyses based on the Bray-Curtis index of dissimilarity between samples, calculated with log-transformed species abundance data (log N + 1). NMDS provides a visual representation of the dissimilarity in carabid beetle species composition between samples (Shepard, 1962), whereas Permanova uses permutations of the data to provide significance tests for the independent variables (Anderson, 2001), habitat type and sampling period in our case. Furthermore, in order to test if carabid assemblages in field defects and boundaries represented a distinct set of species or a subset of the species present in OSR crop, we calculated the matrix temperature. This metric measures the degree of nestedness on species per sites matrices and values can range from 0 to 100°, with low temperatures indicating higher degrees of nestedness and high temperatures random distributions of species among sites (Atmar and Patterson, 1993). We calculated matrix temperature separately for each of the 20 fields to measure local nestedness among habitats. These analyses were performed in R with the package vegan (Oksanen et al., 2007). Finally, we performed an Indicator Species analysis with the R package indicspecies (De Caceres and Legendre, 2009) to determine if there were ground beetle species closely linked to field defects, OSR fields, or boundaries between the two. To analyse the effects of field defect characteristics on carabid assemblages, we calculated the difference in activity-density and species richness between field defects and field interiors. We used mean activity-density of the three traps per habitat and the accumulated species richness to calculate these variables. Differences in activity-density and species richness between field defects and field interiors were used as response variables in LMMs with a normal distribution, and field as a
2.2. Data collection To investigate the effects of field defects on activity-density (number of collected individuals), species richness and species composition, carabid beetles were sampled using pitfall traps. Carabid beetles were collected in two sampling periods (each 21 days long) from late May to June 11 and from June 12 to early July. The timing was selected to cover different phenological phases of the crop (flowering vs. seed maturation). In total, 180 pitfall traps were operated during each sampling period. Pitfall traps were made of 400 ml plastic cups, dug into the soil with the rim of the cup flush with the soil surface (9.5 cm in diameter). All cups were filled with 200 ml of propylene glycolwater solution (1:3, v/v) as a killing and preservative fluid. This fluid is efficient for collecting carabid beetles and is relatively non-toxic to nontarget organisms (Knapp and Ruzicka, 2012). Pitfall traps were covered by roofs made of an aluminium sheet (25 × 35 cm) to prevent flooding during heavy rainfall and to protect the traps from damage by large mammals (e.g., wild boars and roe deer). Roofs were placed 5 cm above the openings of the cups using three long nails. Shallow ditches were dug around traps along the slope to prevent flooding from water flowing over the surface. A set of three pitfall traps arranged 5 m apart were installed in three habitats per field: 1) field defect (central part); 2) boundary between the crop and field defect; 3) field interior (area with well-developed OSR plants). In total, nine pitfall traps were exposed per field in each period. Fifteen traps out of 360 were damaged or destroyed by wild boars and foxes. Samples originating from damaged or destroyed traps were omitted from our analyses. In all cases at least one trap out of three installed per habitat type remained undamaged. After sample collection, surplus preservation fluid was removed by sieving in the field and pitfall trap samples were transported to the laboratory. Pitfall samples were placed individually into plastic bags, and were coded and stored in at −20 °C until processing. Later, all carabid beetles were extracted from the pitfall samples and identified to species using the identification guide by Hůrka (1996). In early May, field defects were almost without any vegetation (weed cover) but some of them started to become overgrown during the following weeks. We measured the vegetation cover of each field defect between the first and second sampling period using a visual estimation of the proportion of bare ground and vegetation cover. In order to reduce sampling bias, the same observers (MS and MK) performed these estimations. At the same time, the size (diameter) of each field defect was directly measured using a tape measure. 2.3. Statistical analyses Statistical analyses are based on 345 data points representing 3
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defects (Fig. 3a; Tukey´s t-tests p < 0.001 for boundaries and field interiors). More carabid species were recorded in the summer than in the spring period (mean 5.6 ± 0.2 in spring vs. 8.0 ± 0.2 in summer; Fig. 3a), which corresponded well to the pattern observed for activitydensity. The interaction between habitat type and sampling period was not significant (GLMM: χ22,337 = 2.64; p = 0.27).
random variable. Independent variables were field defect size (logarithm of the diameter), proportion of vegetation cover, sampling period and the paired interactions between these variables. Model selection was performed as explained above. The analyses were performed using the R package nlme (Pinheiro et al., 2013). 3. Results
3.3. Species composition In total, 27 076 carabid beetles of 75 species were collected (Appendix A3). We registered a shift in the dominant species across the habitat types. The three most common species in field defects were Poecilus cupreus (2467 individuals), Brachinus crepitans (1136 individuals) and Pterostichus melanarius (943 individuals), whereas the most common species in boundaries were Poecilus cupreus (2754 individuals), Brachinus crepitans (1572 individuals) and Anchomenus dorsalis (1458 individuals), and in field interiors the most common species were Anchomenus dorsalis (2583 individuals), Poecilus cupreus (2143 individuals) and Amara ovata (2076 individuals). This clearly indicated that some abundant species were avoiding field defects, e.g., Anchomenus dorsalis and Amara ovata, whereas other kept their activitydensity in field defects comparable to surrounding OSR crop, e.g., Poecilus cupreus, or even increased their activity-density in field defects and defect boundaries, e.g., Harpalus signaticornis (Appendix A3).
Multivariate analyses of species composition showed differences between habitat types and sampling periods (Fig. 4). The Permanova indicated significant effects of habitat type (F1,337 = 20.00; p = 0.001; R2 = 0.10), sampling period (F1,337 = 25.15; p = 0.001; R2 = 0.06), and their interaction (F1,337 = 3.53; p = 0.001; R2 = 0.02) on carabid species composition. The NMDS bi-plot indicate a significant gradient from field defect samples to field interiors in the first NMDS axis (Fig. 4). The difference in species composition between field defects and other habitat types was caused mainly by reduced numbers of several abundant species in field defects, e.g., Amara ovata, Amara similata, Anchomenus dorsalis and Brachinus explodens (Appendix A3). The nestedness analysis resulted in low mean matrix temperature per field (only 3.81° ± 0.37), indicating a high degree of nestedness among habitats. Indicator Species analysis confirmed that only Bembidion quadrimaculatum was associated with field defects, Bembidion lampros and Microlestes minutulus were linked to field defects and boundaries, and the four abundant species mentioned above (Anchomenus dorsalis, Amara ovata, Amara similata, and Brachinus explodens) were associated with boundaries and OSR crops (Appendix A4).
3.1. Activity-density Total carabid activity-density was significantly influenced by habitat type (GLMM: χ22,336 = 21.87; p < 0.001), sampling period (GLMM: χ21,336 = 178.12; p < 0.001), and the interaction between habitat type and sampling period (GLMM: χ22,336 = 15.14; p < 0.001; Fig. 3b). In spring, activity-density was significantly lower in field defects than in field interiors (Tukey´s t test, p = 0.002) or boundaries (Tukey´s t test, p = 0.005), whereas no differences between field interiors and boundaries were found (Tukey´s t test, p = 0.97). In summer, activity-density increased in all three habitat types (mean 43.7 ± 4.8 in spring vs. 113.9 ± 8.5 in summer). Similarly to spring, activity-density was lowest in field defects (Tukey´s t-tests, p < 0.001 for both boundaries and field interiors). However, there was also a tendency for marginally higher activity-density in field interiors compared to boundaries (Tukey´s t test, p = 0.06).
3.4. Effects of field defect characteristics The difference in carabid activity-density between field defects and crop interiors was affected by the sampling period (LME: F1,37 = 13.06; p = 0.002). The difference was higher in summer due to the relatively higher activity-densities in crop interiors at this time (see Section 3.1). There were no significant effects of field defect size, vegetation cover, and interactions between sampling period and defect size or vegetation cover on the difference in carabid activity-density between field defects and crop interiors (Appendix A5). This indicates that even very small field defects reduced carabid activity-density in their central parts. The difference in carabid beetle richness between field defects and crop interiors decreased significantly with the increasing proportion of vegetation cover in field defects (LME: F1,37 = 7.92; p = 0.012; Fig. 5). Note that field defects with more than 80 % of vegetation cover hosted similar numbers of carabid species as OSR field interiors. Field defect size, sampling period, and the interaction between these variables were not important for the difference in carabid species richness between
3.2. Species richness Carabid species richness was affected by habitat type (GLMM: χ22,339 = 22.91; p < 0.001) and sampling period (GLMM: χ21,339 = 71.87; p < 0.001). Species richness was similar in field interiors and habitat boundaries (Tukey´s t-test p = 0.83), but significantly lower in field
Fig. 3. Effects of habitat type and sampling period on (a) species richness and (b) activity-density of carabid beetle assemblages in oilseed rape fields. Predictions of the best GLMMs (mean ± 95 % confidence intervals) are shown. 4
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Fig. 4. Effects of habitat type on species composition of carabid beetle assemblages. Non-metric multidimensional scaling ordination diagram based on species abundances (log-transformed) is shown. Habitat types represented are: field defects (D; red), boundaries (B; black), and oilseed rape field interiors (F; green). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
second (summer) period. The bare ground was directly exposed to sunshine and local temperatures within field defects were thus much higher than in OSR field interiors (Appendix A6). Many carabid species cannot tolerate even short-term exposure to temperatures over 50 °C (Thiele, 1977; Slatyer and Schoville, 2016). Vegetation-free soil also dries out faster, and water availability seems to be a limiting factor for carabids (Thiele, 1977; Holland, 2002). Water availability is also crucial for plant growth, thereby slowing down the development of vegetation within field defects during summer. Low abundance of plants has a direct negative effect on abundance of herbivores and detritivores, and thus reduces potential food sources for carabids (Cameron and Leather, 2012). Field defects thus look like low productivity islands within arable fields. Several studies focused on carabid beetle assemblages inhabiting non-crop habitats within arable fields show that carabid activity-density and species richness can be positively related to habitat productivity (Eyre et al., 2013; Knapp and Rezac, 2015). Bare soil could also increase the predation risk experienced by carabid beetles themselves (Blubaugh et al., 2017). Vertebrate predators as well as arthropod intra-guild competitors of carabid beetles, e.g., spiders and ants, can be more effective in vegetation-free field defects than in field defects with dense vegetation (Lovei and Sunderland, 1996). On the other hand, field defect boundaries are a quite attractive habitat to many carabid species. For several species the highest activitydensity was recorded at boundaries (Appendix A3) and overall carabid species richness peaked at boundaries between field defects and field interiors. This finding is in line with studies that recorded positive edge effects on carabid assemblages observed at boundaries between arable fields and neighbouring permanent non-crop habitats (Magura et al., 2017; Knapp et al., 2019). Both spillover between neighbouring habitats and existence of edge specialist species can be responsible for the observed pattern (Knapp et al., 2019).
Fig. 5. Effects of plant cover within field defects on the difference in species richness of carabid beetles between field defects and field interiors. The slope (black line) and 95 % confidence interval (grey band) estimated from the best LMM are shown.
field defects and crop interiors (Appendix A5). 4. Discussion 4.1. Summary of main results In general, field defects seem to be suboptimal habitats for carabid beetles inhabiting Central European OSR fields. Contrary to our prediction that field defects within OSR fields will significantly enhance local activity-density and diversity of carabids via increased habitat heterogeneity, both activity-density and species richness were higher within OSR crop interiors compared to field defects. We recorded higher activity-density and species richness in the summer period compared to spring. Carabid activity-density tended to be highest within OSR crop interiors, whereas carabid species richness tended to peak on the boundary between OSR crop and field defect. Only a few carabid species occurred more frequently in field defects than in the surrounding crop. Our results also indicate that the spatial distribution of carabid beetles within OSR crops with field defects varied over time.
4.3. Do field defects represent unique and valuable habitats for carabids? Landscape heterogeneity and the presence of non-crop habitats in agroecosystems is one of the most important factors affecting local biodiversity and provision of ecological services (Bianchi et al., 2006; Gonzalez et al., 2017). Even species-poor habitats hosting unique species can increase species richness at the landscape level (Knapp and Rezac, 2015). Our results suggest that carabid diversity can be slightly enhanced at boundaries between OSR crops and field defects. However, carabid assemblages in field defects did not differ from boundary and field interior assemblages by the presence of many unique species, but rather the activity-density of several dominant species was reduced
4.2. Field defect effects on activity-density and species richness Factors affecting the presence of carabid beetles in field defects are probably related to abiotic characteristics of this specific habitat. The investigated field defects were predominantly covered by bare ground in the first (spring) sampling period and some of them even in the 5
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Funding
there. Three small carabid species Bembidion quadrimaculatum, Bembidion lampros and Microlestes minutulus were identified as the indicator species typical for field defects; indeed, these species were quite rare in our study system (only 20, 131 and 18 individuals were collected, respectively). Thus, contrary to our expectations, field defects hosted mainly impoverished carabid assemblages from the OSR crop with very few species unique to field defects. This conclusion is also supported by a very high nestedness of carabid assemblages within arable fields investigated in our study.
This study was supported by the Internal Grant Agency of Faculty of Environmental Sciences, Czech University of Life Sciences Prague (grant number 42110/1312/3118) and the Czech Science Foundation (grant number 18-26542S). Declaration of Competing Interest None.
4.4. How to improve field defects
Acknowledgments
Field defects with a high weed cover hosted carabid assemblages with their species richness comparable to those in OSR crop interiors, but field defects with a high proportion of bare ground hosted speciespoor carabid assemblages. This fact supports the idea of vegetating large field defects, a practice already followed by some Czech farms (Fig. 1b). Planting nectar-rich plant communities there would also be beneficial to pollinators and other insects. Support of such activities by an agri-environmental scheme (AES) could be a possibility. On the other hand, bare ground can be more than 10 °C warmer compared to field interiors (Balisky and Burton, 1995), also supported by our measurements; see Appendix A6), which is detrimental in peaking summer, but can be beneficial for ectothermic animals in early spring and on cold days (Key, 2000). Moreover, bare soil can also be a suitable habitat for some solitary bees and wasps for nesting, and a good hunting place for other beneficial insects (Fry and Lonsdale, 1991). However, nearby vegetation seems to be necessary (Mazia et al., 2006; Cameron and Leather, 2012) and thus small areas of bare ground in defects predominantly covered by vegetation might be ideal. Especially in the case of large field defects, Czech farmers sometimes re-sow field defects with other crops that improve soil quality, e.g., legumes. This indicates that re-sowing practice can be quite easily adopted by farmers even without subsidies (specific AES; see Fig. 1b). However, future studies are needed to compare biodiversity of bare and re-sown field defects across multiple taxa to determine if re-sowing is the best management strategy in all cases. Considering the relevance of bare ground for some insects (Key, 2000), the combination of re-sowing most of the area and leaving strips of bare ground around could be most suitable solution for enhancing biodiversity within field defects. Note also that field defects with naturally developed weedy vegetation can host rare and threatened plant species (Appendix A2) and also bird populations are enhanced in similar habitats called “lark windows” in Germany (Oberwelland and Nottmeyer-Linden, 2009). Therefore, we predict that re-sowing all field defects can be used only in specific cases and at least some field defects should remain without any intervention.
We would like to thank the owners of the fields for their permission to perform fieldwork, Jana Zemanová for her help in field, Martin Štrobl for his help in laboratory, Tiit Teder for helpful comments on the previous version of our manuscript and Mark Francis Sixsmith for language corrections. We are grateful to three anonymous reviewers for their insightful and constructive suggestions that helped to improve our manuscript. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2020.106856. References Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26, 32–46. Atmar, W., Patterson, B.D., 1993. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382. Balisky, A.C., Burton, P.J., 1995. Root-zone soil-temperature variation associated with microsite characteristics in high-elevation forest openings in the interior of BritishColumbia. Agric. For. Meteorol. 77, 31–54. Batary, P., Baldi, A., Kleijn, D., Tscharntke, T., 2011. Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc. R. Soc. B-Biol. Sci. 278, 1894–1902. Bates, D., Machler, M., Bolker, B.M., Walker, S.C., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188. Bianchi, F.J.J.A., Booij, C.J.H., Tscharntke, T., 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B 273, 1715–1727. Blitzer, E.J., Dormann, C.F., Holzschuh, A., Klein, A.-M., Rand, T.A., Tscharntke, T., 2012. Spillover of functionally important organisms between managed and natural habitats. Agric. Ecosyst. Environ. 146, 34–43. Blubaugh, C.K., Widick, I.V., Kaplan, I., 2017. Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels. Oecologia 185, 1–11. Boetzl, F.A., Krimmer, E., Krauss, J., Steffan-Dewenter, I., 2019. Agri-environmental schemes promote ground-dwelling predators in adjacent oilseed rape fields: Diversity, species traits and distance-decay functions. J. Appl. Ecol. 56, 10–20. Bohan, D.A., Boursault, A., Brooks, D.R., Petit, S., 2011. National-scale regulation of the weed seedbank by carabid predators. J. Appl. Ecol. 48, 888–898. Brose, U., 2003a. Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135, 407–413. Brose, U., 2003b. Island biogeography of temporary wetland carabid beetle communities. J. Biogeogr. 30, 879–888. Brose, U., 2003c. Regional diversity of temporary wetland carabid beetle communities: a matter of landscape features or cultivation intensity? Agric. Ecosyst. Environ. 98, 163–167. Cameron, K.H., Leather, S.R., 2012. Heathland management effects on carabid beetle communities: the relationship between bare ground patch size and carabid biodiversity. J. Insect Conserv. 16, 523–535. Cassman, K.G., 1999. Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. PNAS 96, 5952–5959. Dainese, M., Schneider, G., Krauss, J., Steffan-Dewenter, I., 2017. Complementarity among natural enemies enhances pest suppression. Sci. Rep. 7, 8172. De Caceres, M., Legendre, P., 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90, 3566–3574. Djoudi, E., Plantegenest, M., Aviron, S., Petillon, J., 2019. Local vs. landscape characteristics differentially shape emerging and circulating assemblages of carabid beetles in agroecosystems. Agric. Ecosyst. Environ. 270, 149–158. Emmerson, M., Morales, M.B., Onate, J.J., Batry, P., Berendse, F., Liira, J., Aavik, T., Guerrero, I., Bommarco, R., Eggers, S., Part, T., Tscharntke, T., Weisser, W., Clement,
5. Conclusion Natural field defects within OSR fields hosted less species-rich carabid assemblages compared to assemblages in OSR crop and boundaries. Moreover, the activity-density of several dominant carabid species was strongly reduced in field defects and only a few carabid species were more abundant there. Thus, the avoidance of even very small field defects confirms the ability of carabid species to be used as bioindicators of habitat quality, even at very small scales (Brose, 2003a, c; Rainio and Niemela, 2003; Knapp and Rezac, 2015). Importantly, the positive influence of vegetation cover on carabid richness in field defects indicates that re-sowing field defects or supporting natural weed communities can be a useful habitat management measure to support carabids within arable fields. However, future research is needed to determine if field defects support other groups of beneficial or endangered arthropods and to confirm whether re-sowing will also improve field defect quality for them. 6
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M. Seidl, et al.
Rep. 9, 8967. Lovei, G.L., Magura, T., 2017. Ground beetle (Coleoptera: Carabidae) diversity is higher in narrow hedges composed of a native compared to non-native trees in a Danish agricultural landscape. Insect Conserv. Divers. 10, 141–150. Lovei, G.L., Sunderland, K.D., 1996. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu. Rev. Entomol. 41, 231–256. Magura, T., Lovei, G.L., Tothmeresz, B., 2017. Edge responses are different in edges under natural versus anthropogenic influence: a meta-analysis using ground beetles. Ecol. Evol. 7, 1009–1017. Mazia, C.N., Chaneton, E.J., Kitzberger, T., 2006. Small-scale habitat use and assemblage structure of ground-dwelling beetles in a Patagonian shrub steppe. J. Arid Environ. 67, 177–194. Oberwelland, C., Nottmeyer-Linden, K., 2009. Praktische Schutzmaßnahmen für Feldvögel. Nat. NRW 3, 31–33. Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, H.M.H., 2007. The vegan package. Community Ecol. Package 10, 631–637. Pakeman, R.J., Stockan, J.A., 2014. Drivers of carabid functional diversity: abiotic environment, plant functional traits, or plant functional diversity? Ecology 95, 1213–1224. Pardon, P., Reheul, D., Mertens, J., Reubens, B., De Frenne, P., De Smedt, P., Proesmans, W., Van Vooren, L., Verheyen, K., 2019. Gradients in abundance and diversity of ground dwelling arthropods as a function of distance to tree rows in temperate arable agroforestry systems. Agric. Ecosyst. Environ. 270, 114–128. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Development Core Team, R., 2013. Nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3. pp. 1–107. Pollard, K.A., Holland, J.M., 2006. Arthropods within the woody element of hedgerows and their distribution pattern. Agric. For. Entomol. 8, 203–211. R Development Core Team, 2017. A Language and Environment for Statistical Computing. Available at. http://www.R-project.org. Rainio, J., Niemela, J., 2003. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers. Conserv. 12, 487–506. Rand, T.A., Tylianakis, J.M., Tscharntke, T., 2006. Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol. Lett. 9, 603–614. Saska, P., Vodde, M., Heijerman, T., Westerman, P., van der Werf, W., 2007. The significance of a grassy field boundary for the spatial distribution of carabids within two cereal fields. Agric. Ecosyst. Environ. 122, 427–434. Shepard, R.N., 1962. The analysis of proximities: multidimensional scaling with an unknown distance function. Psychometrika 27, 125–140. Slatyer, R.A., Schoville, S.D., 2016. Physiological limits along an elevational gradient in a radiation of montane ground beetles. PLoS One 11, e0151959. Thiele, T.U., 1977. Carabid Beetles in Their Environments: a Study on Habitat Selection by Adaptations in Physiology and Behaviour. Springer-Verlag. Thomas, M.B., Wratten, S.D., Sotherton, N.W., 1991. Creation of island habitats in farmland to manipulate populations of beneficial arthropods – predator densities and emigration. J. Appl. Ecol. 28, 906–917. Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001. Forecasting agriculturally driven global environmental change. Science 292, 281–284. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol. Lett. 8, 857–874. Tschumi, M., Albrecht, M., Collatz, J., Dubsky, V., Entling, M.H., Najar-Rodriguez, A.J., Jacot, K., 2016. Tailored flower strips promote natural enemy biodiversity and pest control in potato crops. J. Appl. Ecol. 53, 1169–1176. Varchola, J.M., Dunn, J.P., 2001. Influence of hedgerow and grassy field borders on ground beetle (Coleoptera: Carabidae) activity in fields of corn. Agric. Ecosyst. Environ. 83, 153–163.
L., Bengtsson, J., 2016. How agricultural intensification affects biodiversity and ecosystem services. In: Dumbrell, A.J., Kordas, R.L., Woodward, G. (Eds.), Advances in Ecological Research, Vol 55: Large-Scale Ecology: Model Systems to Global Perspectives, pp. 43–97. Eyre, M.D., Luff, M.L., Leifert, C., 2013. Crop, field boundary, productivity and disturbance influences on ground beetles (Coleoptera, Carabidae) in the agroecosystem. Agric. Ecosyst. Environ. 165, 60–67. Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C., Siriwardena, G.M., Martin, J.L., 2011. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol. Lett. 14, 101–112. Firbank, L.G., Petit, S., Smart, S., Blain, A., Fuller, R.J., 2008. Assessing the impacts of agricultural intensification on biodiversity: a British perspective. Phil. Trans. R. Soc. B 363, 777–787. Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574. Fry, R., Lonsdale, D., 1991. Habitat Conservation for Insects: a Neglected Green Issue. Amateur Entomologists’ Society. Fusser, M.S., Holland, J.M., Jeanneret, P., Pfister, S.C., Entling, M.H., Schirmel, J., 2018. Interactive effects of local and landscape factors on farmland carabids. Agric. For. Entomol. 20, 549–557. Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhoffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyorgyi, H., Viana, B.F., Westphal, C., Winfree, R., Klein, A.M., 2011. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 14, 1062–1072. Gayer, C., Lovei, G.L., Magura, T., Dieterich, M., Batary, P., 2019. Carabid functional diversity is enhanced by conventional flowering fields, organic winter cereals and edge habitats. Agric. Ecosyst. Environ. 284, 106579. Geiger, F., Wackers, F., Bianchi, F., 2009. Hibernation of predatory arthropods in seminatural habitats. Biocontrol 54, 529–535. Gonzalez, E., Salvo, A., Valladares, G., 2015. Sharing enemies: evidence of forest contribution to natural enemy communities in crops, at different spatial scales. Insect Conserv. Divers. 8, 359–366. Gonzalez, E., Salvo, A., Valladares, G., 2017. Arthropod communities and biological control in soybean fields: forest cover at landscape scale is more influential than forest proximity. Agric. Ecosyst. Environ. 239, 359–367. Harvey, J.A., van der Putten, W.H., Turin, H., Wagenaar, R., Bezemer, T.M., 2008. Effects of changes in plant species richness and community traits on carabid assemblages and feeding guilds. Agric. Ecosyst. Environ. 127, 100–106. Holland, J.M., 2002. The Agroecology of Carabid Beetles. Intercept, Andover, UK. Hůrka, K., 1996. Carabidae of the Czech and Slovak Republics. Carabidae České a Slovenské republiky, Kabourek, Zlín. Key, R., 2000. Bare ground and the conservation of invertebrates. Br. Wildl. 2, 183–191. Kleijn, D., Baquero, R.A., Clough, Y., Diaz, M., De Esteban, J., Fernandez, F., Gabriel, D., Herzog, F., Holzschuh, A., Johl, R., Knop, E., Kruess, A., Marshall, E.J.P., SteffanDewenter, I., Tscharntke, T., Verhulst, J., West, T.M., Yela, J.L., 2006. Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol. Lett. 9, 243–254. Knapp, M., Rezac, M., 2015. Even the smallest non-crop habitat islands could be beneficial: distribution of carabid beetles and spiders in agricultural landscape. PLoS One 10, e0123052. Knapp, M., Ruzicka, J., 2012. The effect of pitfall trap construction and preservative on catch size, species richness and species composition of ground beetles (Coleoptera: Carabidae). Eur. J. Entomol. 109, 419–426. Knapp, M., Seidl, M., Knappova, J., Macek, M., Saska, P., 2019. Temporal changes in the spatial distribution of carabid beetles around arable field-woodlot boundaries. Sci.
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