Ground beetle (Coleoptera, Carabidae) life history traits as indicators of habitat recovering processes in postindustrial areas

Ecological Engineering 142 (2020) 105615

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Ground beetle (Coleoptera, Carabidae) life history traits as indicators of habitat recovering processes in postindustrial areas

T

Renata Kędziora, , Artur Szwaleca, Paweł Mundałaa, Tomasz Skalskib ⁎

a

Department of Ecology, Climatology and Air Protection, Faculty of Environmental Engineering and Land Surveying, University of Agriculture in Krakow, al. Mickiewicza 24/28, 30-059 Krakow, Poland b Biotechnology Centre, Silesian University of Technology, Gliwice, Poland

ARTICLE INFO

ABSTRACT

Keywords: Carabidae Afforestation Spontaneous succession Life traits Recolonization Landfill

The recovery of postindustrial ecosystems is difficult to predict and depends on numerous factors. Afforestation whereby trees are planted without improvement of soil properties is a popular means of landfill reclamation in Europe, to inhibit the effect of soil erosion. This slows down or completely prevents effective recolonization of many natural ecosystem components. The aim of the study was to test a method using the life-history traits of ground beetle assemblages as a predictor of the effectiveness of ecological restoration in afforested areas. The study was conducted on 45 sampling transects located in three ecosystem types: afforested landfills, landfills where spontaneous succession took place and reference forests. The following carabid life history traits were analysed: body size, dispersal power, food preferences, breeding type, and habitat preferences. In total, 2036 specimens belonging to 36 Carabidae species were collected. Non-metric multidimensional scaling was used to classify ground beetle assemblages according to ecosystem types (analysis of dissimilarity showed significant distance differences, p < .001). We noted shifts in life history traits towards early succession in assemblages of afforested areas. Generalized linear mixed models of afforested sites revealed significantly higher abundance of herbivorous, open-area species with medium body size, high dispersal power and a spring breeding cycle. In contrast, sites where spontaneous succession occured were dominated by carabids whose life history traits were similar to those of assemblages inhabiting the reference forests, i.e. medium body-sized predators with low dispersal power and an autumn breeding cycle. We conclude that an approach based on ground beetle lifehistory traits can be a useful tool indicating the direction and effectiveness of ecosystem recovery in postindustrial areas and can be used as a measurable criterion for assessment of restoration activities.

1. Introduction Much attention has been devoted to ecosystem recovery in areas with a high level of industrial activity, mainly due to the area they occupy on a global scale (Tropek and Prach, 2012; Moradi et al., 2018). The conceptual planning of ecosystem recovery must include both restoration objectives and measurable success criteria. Establishment of measurable criteria of restoration success is difficult due to the numerous ecosystem characteristics that must be considered (Hobbs et al., 2009). Tree planting is known to be essential for restoring degraded lands (Lamb et al., 2005). However, in such areas particular attention should be focused not only on vegetation but also on the promotion of habitat conditions increasing the success of species recolonization. There is a need for a method of assessing ecological processes for the purpose of judging restoration success. Post-industrial reclamation

⁎

procedures generally comprise two main activities: spontaneous succession, which reflects natural ecological processes and afforestation, that rapidly changes the structure of plant cover (Schulz and Wiegleb, 2000; Hadčová and Prach, 2003). Post-industrial areas are subject to natural regeneration processes resulting in the development of new and often specific habitat conditions for biota (Haigh, 2000; Hobbs et al., 2009; Lundholm and Richardson, 2010; Laarmann et al., 2015). In other cases, reclamation procedure are carried out to neutralize the negative effects of industrial activity, most often involving tree planting or soil remediation of degraded land (Mulligan et al., 2001; Zipper et al., 2011; Laarmann et al., 2015). In both cases ecosystem recovery is unpredictable and depends on numerous factors, such as soil parameters (Hendrychová et al., 2012), microclimatic factors, or the suitability of refuges for potential recolonizing species (Prach et al., 2007). The surrounding land-use

Corresponding author. E-mail address: [email protected] (R. Kędzior).

https://doi.org/10.1016/j.ecoleng.2019.105615 Received 18 December 2018; Received in revised form 12 September 2019; Accepted 28 September 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.

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Fig. 1. The map of the study areas and location of the sampling transects.

matrix and the suitability of such environmental factors are often limited in degraded industrial areas, that slows down or prevents effective recolonization by plants and animals (Niemelä, 2001; Topp et al., 2001; Frouz et al., 2008). For this reason, increasing attention is focused on restoration of mechanisms ensuring efficient ecosystem function e.g. improvement of trophic chains, mutualistic relations, and productivity (Frouz et al., 2006). Many studies confirm that the use of selected species or taxa (plants as well as invertebrates) as bioindicators of environmental disturbances contributes to understanding of the mechanisms and success of reclamation practices (Ribas et al., 2012; Tropek et al., 2012; Piekarska-Stachowiak et al., 2014; Tropek et al., 2014; Šebelíková et al., 2016). One of the best described groups of soil invertebrate bioindicators of post-industrial ecosystems is carabid beetles (Koivula, 2011; Skalski et al., 2015). Carabids are highly diverse and sensitive to disturbances. Their taxonomy and ecology are well known. They are top predators in the soil layer with diverse habitat preferences (from very narrow to very broad), participating in a number of ecosystem processes, such as herbivory, predation, granivory and mediation of nutrient flows (Loreau, 1995). The structure of carabid assemblages has been shown to respond to disturbances such as river degradation (Skalski et al., 2016a), agricultural practices (Kosewska et al., 2016), or forest management (Skłodowski, 2014). In areas transformed by industrial activity, community indices such as species composition and diversity, abundance or species richness have been used to determine the state of the natural environment (Skalski and Pośpiech, 2006; Kędzior et al., 2014). However, these indicies do not clearly define the ecological state of post-industrial areas (Skalski et al., 2011). A more detailed characterization of assemblages based on of life-history traits more precisely reveals the mechanism of the functioning of recovering ecosystems (Vandewalle et al., 2010; Ng et al., 2018). High dispersal power (most species with flight ability), body size modifications (towards smaller

species) and high reproductive potential (most species with a flexible spring breeding strategy) indicate a high disturbance level in the ecosystem (Barbaro and Van Halder, 2009; Gerisch, 2011; Skalski et al., 2016a; Kędzior, 2018; Nolte et al., 2019). Moreover, attention should be focused on trophic relationships in these ecosystems, where abundance of predators decreases due to the absence of detritivores (e.g. earthworms and springtails), while the proportion of herbivores increases. This is indicative of disruptions in food webs and a reduced decomposition rate. Carabid are an important element of efficient circulation of matter and energy flow (Loreau, 1995; Skalski et al., 2011; Schirmel et al., 2012). Life-history traits are subject to natural selection and can be used to explain the occurrence of species in habitat (Nolte et al., 2019). In the case of ground beetle assemblages, commonly analysed life traits include body size, dispersal power, food preferences, and breeding strategy (Pedley and Dolman, 2014; Bell et al., 2017; Kędzior et al., 2018). In habitats recovering after a disturbance, primarily smallbodied species with high dispersal power and high ecological flexibility appear. On the other hand, the proportion of carabid habitat specialists increases with time after the disturbance (Skalski et al., 2016a). Therefore the presence or absence of individual ecological groups, but also the distribution of their abundance, indicate the course of processes taking place in the entire ecosystem and can be useful in assessment of restoration success or monitoring of recovered areas (Skalski et al., 2016b; Bell et al., 2017). The aim of the study was to assess the effectiveness of two of the most common types of recovery (spontaneous succession and afforestation) based on variation in ground beetle life-history traits. We hypothesized that carabid life-history traits in effectively restored ecosystems should tend towards reference forest systems. Conversely, we also hypothesized that ineffective restoration of ground beetle communities would be characterized by pioneer colonizers, mainly 2

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small-sized species with high dispersal power, broader trophic preferences, and more flexible breeding strategies after several years of recovery. We expected that if the trophic chains were disturbed, we should observe a shift in trophic preferences towards herbivory and a decline in the abundance of forest specialist predators.

2.2. Study design and ground beetle sampling To estimate how the carabid communities differ between spontaneous succession and reclaimed sites, all sampling transects were located in late forest dominated stands (> 20 years old) (Prach et al., 2007; Chazdon, 2008). We chose three ecosystem types to examine (afforested, spontaneous succession and reference forest). Two landfill areas and two reference forests were estimated for each type. The distances between them were > 5 km. Five to ten replicates of pitfall trap transects were established in homogenous woodlands (canopy cover above 80%) in each area. The number of transects depended on tree species homogeneity, tree age structure, and seedlings cover. To eliminate the ecotone effect, the transects were placed at least 50 m from the edge of the habitat (Yu et al., 2007). The mean distance between transects was 200 m. In total 45 sampling transects were established in three ecosystem types replicated in two areas. Each transect consisted of 5 traps positioned 10 m apart. The traps were plastic cups, 7 cm in diameter and 10 cm high, placed flush with the soil surface, 10 m apart, and 1/3 filled with ethylene glycol. Overall 225 pitfall traps were installed. They were inspected four times during the growing season, monthly from May to June and from September to mid-October in 2013 (Skawina landfill) and 2015 (other landfills). Data from the five traps in each transect and four collection periods were pooled. The ground beetles were identified to species level according to Hurka (1996). Individual species were classified according to the following life-history traits: body size, dispersal power, food preferences, breeding strategy, and habitat preferences. The classification according to body size was as follows: species with small body size (< 8 mm), medium body size (8–15 mm) and large body size (> 15 mm). Depending on dispersal power, the carabid species were classified as brachypterous (with no or reduced wings), dimorphic or macropterous species. To analyse the feeding strategy of ground beetles, they were divided into predators (preying exclusively on invertebrates) and herbivores (diet consists mainly of plants). Carabid beetles were also divided into two main breeding groups: autumn breeders (eggs laid mainly during the first weeks of autumn; females require nearly the entire season to mature and lay eggs) and spring breeders (eggs are laid from March to May; females mature just after overwintering). Ground beetles were classified into two types according to habitat preferences: open-area specialists and forest species (Thiele, 1997; Skalski et al., 2016b; Bell et al., 2017). All morphological and ecological carabid traits were taken from Hurka (1996).

2. Materials and methods 2.1. Study area The study was conducted in Lesser Poland, an industrial region of southern Poland. Heavy industrial activity in this region began at the end of the 19th century, associated mainly with the rapid growth of the cities of Krakow and Jaworzno. The study was carried out on four post-industrial landfills, Trzebionka (50°09′ N, 19°25′ E), Skawina (49°58′ N, 19°46′ E), Siersza (50°13′ N, 19°27′ E) and Krze (50°10′ N, 19°27′ E), surrounded by agricultural (crops and meadows), urbanized, and industrial areas (Fig. 1). They operated from the first half of the 20th century until 2005. The matter deposited on the landfills consisted mainly of a mixture of tailings and weathered fine-grained sludge and ashes. During deposition, the coarsest fraction of the landfills was used to build the embankments by means of clay grouting (Graf, 1969). The effectiveness of landfill restoration is mainly determined by the recovery procedures, and by the species composition and age of the dominant trees (Laarmann et al., 2015; Šebelíková et al., 2016), so these parameters were controlled with respect to vegetation structure parameters (canopy closure, tree cover, tree diameter, and tree height). We also measured other vegetation parameters which can differ between recovery types (cover of shrubs, seedlings, herbs, and moss; and number of species trees, shrubs, and herbs). Two main recovery types prevail in the study area: (1) technical reclamation (afforestation) in the Trzebionka and Skawina landfills, by covering slag waste with topsoil and planting trees in regular rows, with a mixture of native (Betula pendula, Populus tremula, and Sorbus aucuparia) and non-native (Robinia pseudoacacia) species of similar age; (2)spontaneous succession with no human intervention in the Siersza and Krze landfills, with a heterogeneous and irregular spatial system of trees mainly of species found in neighbouring stands (Betula pendula, Populus tremula, Sorbus aucuparia, and a small number of Pinus silvestris). In addition, two mixed forests (Pino-Quercetalia) were chosen as reference areas (49°57′ N, 19°45′ E; 50°11′ N, 19°30′ E) (Table 1), where Carpinus betulus, Quercus robur and Pinus silvestris were the dominant tree species.

2.3. Environmental variables At each sampling transect, soil material was collected to determine

Table 1 The mean ± SD environmental variables measured for each study area. The minimum and maximum values are provided in the brackets. Abbreviations for ecosystem recovery types: A - afforested, SS - spontaneous succession, and F - reference forest. Environmental variable

Trzebionka

Skawina

Siersza

Krze

Forest 1

Forest 2

Landfill size [ha] Recovery type Cd [mg/kg−1]

64 Afforestation (A) 18.86 (2.3–70.3) 1003.07 (90.5–3306.1) 2925.53 (313.3–8000) 70.64 (22.1–130.8) 7.56 (6.9–7.8) 7.3 (6.8–7.5) 3.87 (2.7–5.3)

47 Afforestation (A) 0.32 (0.2–0.5) 24.9 (12.7–34) 62.25 (47–98) 7.62 (6.1–8.7) 7.6 (7.6–7.7) 7.3 (7.1–7.4) 5.77 (5.3–6.8)

15 Spontaneous succession (SS) 8.04 (0.5–34.6) 465.80 (104–1641.1) 1138.19 (230.9–5274.3) 29.63 (20.2–52.2) 7.26 (6.1–8) 6.98 (5.9–7.7) 10.05 (2.3–20.4)

8 Spontaneous succession (SS) 11.06 (0.7–39.8) 756.64 (52.1–3212.8) 1901.34 (194.3–7475.8) 40.42 (15.9–63.8) 7.32 (6.8–7.8) 7,0 (6.5–7.4) 18.15 (4.5–34.1)

90 Reference forest (F) 0.58 (0.1–0.8) 24.1 (17.4–29.3) 79.5 (66–88) 20.17 (8.4–50.3) 5.3 (5.2–5.9) 4.35 (4.8–5.5) 13.9 (10.5–17.7)

300 Reference forest (F) 12.25 (4.8–18.9) 703.17 (233.3–989.0) 408.15 (450.9–1996.6) 80.92 (18–293.4) 5.45 (4.9–5.6) 5.09 (4–4.7) 13.5 (13.1–13.9)

Pb [mg/kg−1] Zn [mg/kg−1] Cu [mg/kg−1] pH H2O pH KCl Organic matter [%]

3

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Table 2 Mean values of vegetation parameters measured for each recovery type and reference forests, with the results of one-way ANOVA and multiple comparison HSD Tukey test. Abbreviations for ecosystem recovery types: A - afforested, SS - spontaneous succession, and F - reference forest. Vegetation parameter

Canopy closure [%] Tree cover [%] Shrubs cover [%] Seedlings cover [%] Herb cover [%] Moss cover [%] Number of tree species Number of shrub species Number of tree species in seedlings stage Number of herb species Total number of plant species Tree diameter [cm] Tree height [m]

Mean A

84.86 78.93 11.3 3.29 4.17 0.98 3.20 3.80 3.86 7,00 20.46 52.79 28.77

Mean SS

83.25 71.10 28.75 11.74 21.25 0.95 4.20 3.70 3.90 6.85 21.00 53.38 29.87

Mean F

80.80 57.40 23.00 8.93 40.24 0.00 4.00 4.40 4.30 10.20 24.90 84.25 34.19

F

0.8 0.8 1.1 3.3 10.3 1.9 8.7 2.3 0.3 3.7 4.1 5864.7 57.5

p

0.420 0.420 0.345 0.045 0.000 0.158 0.000 0.109 0.676 0.031 0.023 0.000 0.000

Multiple comparison HSD Tukey test A-SS

A-F

SS-F

0.803 0.441 0.001 0.035 0.037 0.997 0.000 0.938 0.997 0.990 0.921 0.939 0.287

0.387 0.019 0.102 0.332 0.000 0.198 0.024 0.213 0.697 0.060 0.027 0.000 0.000

0.677 0.151 0.527 0.731 0.041 0.185 0.753 0.101 0.710 0.034 0.043 0.000 0.000

1988), using Statistica software (StatSoft, 2012). We tested spatial autocorrelation across all sites within a distance of 1000 m between sampling points using SAM v 4.0 (Rangel et al., 2010).

soil parameters that could potentially affect epigeic carabid assemblages. The soil samples were collected at a depth of up to 20 cm relative to mean topsoil cover. In the laboratory, wet mineralization was performed in a mixture of concentrated acids (nitric and perchloric) for extraction of Cd, Pb, Zn and Cu. The total content of these trace elements was determined by FAAS on a Solaar M6 Atomic Absorption Spectrometer. Organic matter content was determined by thermogravimetry, and pH was determined in a KCl suspension by potentiometry (Ostrowska et al., 1991). The vegetation structure was estimated during field inspection. A 20 × 20 m quadrat was established in the centre of each sampling transect. The percentage canopy closure, cover of trees, shrubs, seedlings, herbs and moss, the number of tree, shrub, seedlings and herb species, and the total number of plant species were determined for each quadrat. The tree diameter and tree height were measured as well.

3. Results 3.1. Environmental variables The landfills where the study was conducted were slightly varied in terms of trace element content as well as pH and organic matter (Table 1). ANOVA analysis showed that neither the content of heavy metals (Cd: F = 1.49, p = .217, Pb: F = 1.16, p = .347, Zn: F = 1.17, p = .144, Cu: F = 1.99, p = .105) nor the pH of the substrate and organic matter (pH H2O: F = 1.23, p = .318, pH KCl: F = 1.44, p = .253 and OM: F = 5.39, p = .051) were statistically significantly differentiated by the recovery types.

2.4. Data analysis

3.2. Vegetation cover

To test whether environmental factors were controlled across ecosystem types, ANOVA (StatSoft, 2012) was performed for environmental soil and vegetation characteristics. Non-metric multidimensional scaling (NMDS) was performed to obtain an overview of the differences in composition of the beetle assemblages of the three ecosystem types: afforested (A), spontaneous succession (SS) and reference forests (F). Significance of dissimilarity differences between ecosystem types was tested by ANOSIM on the Bray-Curtis dissimilarities matrix with 499 permutations of the data. The NMDS and ANOSIM were analysed using PAST software (version 3.13) (Hammer et al., 2001). We used generalized linear mixed model (GLMM) to model the relationship between life trait parameters of ground beetles and recovery types (Quinn and Keough, 2002). The life traits of carabids were not normally distributed (Shapiro-Wilk test for normality, p < .001), so we fitted the model to the Poisson distribution. Variables were linked to predictors using a log function (Borges and Hortal, 2009). As a small number of sampling transects per recovery type can lead to low power in detecting trends, instability in parameter estimation, and model over-fitting, we used mixed-effect models to overcome these limitations. Recovery type was regarded as a fixed effect describing life-trait variation. We assessed the relative performance of models using a small-sample second-order bias correction of the Akaike information criterion (AICc) (Yanagihara et al., 2017). The best models are those showing the lowest AICc values, which are most likely to have a consistent relationship with the dependent variable, regardless of the variability they explain (Burnham and Anderson, 2002). Differences between means of carabid life-trait parameters in each recovery type were compared by Bonferroni's multiple comparisons test (Hochberg,

Analysis of vegetation structure revealed differences depending on three ecosystem types (A, SS and F), which significantly affected herb and seedling cover, number of tree and herb species, and total number of plant species, as well as tree diameter and tree height (Table 2). Other vegetation parameters did not differ significantly between ecosystems. Comparison of reclamation and spontaneous succession recovery type (multiple comparison by Tukey's HSD test) revealed the significant differences only for shrubs, seedling and herb cover and for the number of tree species. The differences for tree diameter and tree height were significant only in comparison with reference forests, but not between recovery types. 3.3. Ground beetle responses to recovery type A total of 2036 individuals belonging to 36 species were collected during the study (Table A.1). Harpalus rufipes was the most dominant species in the total sample (17%). The next two most abundant species, Calathus erratus and Pterostichus niger, accounted for 13% and 12% of the assemblage respectively. The species composition of carabids from different ecosystem types revealed distinct differences in species dominance depending on the recovery type. Only one species characteristic of open areas, Harpalus rufipes, was dominant on the afforested landfills (A; 64% of this assemblage), followed by Calathus erratus and Poecilus versicolor (6% each). The distribution of species dominance in the landfills by spontaneous succession (SS) was completely different. Calathus erratus (24%) accounted for the highest abundance of this assemblage, followed by the typical forest species Pterostichus niger 4

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Fig. 2. Non-metric multidimensional scaling ordination of ground beetle assemblages (a) and species distribution (b). Assemblages from individual ecosystem types are designated as follows: A - afforested, SS - spontaneous succession, F - reference forests. The symbols marked particular study landfills (square - Siersza, cross Krze, diamond - Trzebionka, circle - Skawina, inverted triangle - Reference forest 1 and triangle - Reference forest 2).

(17%), Pterostichus oblongopunctatus (8%), Leistus rufomarginatus (8%), Carabus problematicus (6%) and Carabus arcensis (6%). In the forested areas constituting the reference sites, Platynus assimilis was the most abundant (19%), followed by Poecilus versicolor (16%), Carabus arcensis (15%), Pterostichus niger (12%) and Carabus violaceus (10%). Moreover, there were many species with special conservation categories (Table A.1; the genus Carabus and the species Oodes helopioides) collected in the reference forest and the landfills where spontaneous succession occured. Non-metric multidimensional scaling (NMDS) showed clear differences between the assemblages sampled in the recovering ecosystem types and the reference forests (Fig. 2a). The ANOSIM analysis indicated significant differences between the assemblages collected in the afforested and transects by spontaneous succession (R = 0.79, p < .001). Furthermore, carabid assemblages inhabiting naturally regenerating landfills differed significantly from the reference assemblages (R = 0.49, p < .001), although this difference was less clear than in the case of assemblages from the reference areas and afforested landfills (R = 0.99, p < .001). The NMDS analysis also revealed that the recovery type influenced carabid species distribution (Fig. 2b). Species of the genus Carabus, which mainly prefer typical forest habitats (e.g. Carabus coriaceus, Carabus ulrichii and Carabus violaceus) and are highly sensitive to disturbances, were associated with reference areas (F), but in some cases were also components of assemblages on landfills where spontaneous succession was observed (SS) (Carabus granulatus and Carabus cancellatus). In the afforested areas (A), we found mainly species with broader ecological plasticity, which is characteristic for early-succession re-colonizers (Harpalus rufipes, Harpalus affinis, Amara communis, Amara curta and Amara famelica). Spatial autocorrelation of ground beetle abundance and life-history trait parameters between sampling transects was not significant. The only exception was herbivores, which were spatially related and associated with a specyfic landfill (Table 3). This may have been the effect of pioneer species of herbs in the central part of the landfills. GLMMs showed that only small-sized species were not significantly linked to the recovery type, showing higher overdispersion of abundances among sampling transects (Table 4). The results of the generalized linear mixed model for carabid lifehistory traits indicated that all parameters analysed were significantly dependent on the ecosystem type (A, SS or F). Figs. 3 and 4 show the distribution of mean carabids abundance broken down by life trait parameters (body size, wing morphology, food preferences, breeding type and habitat preferences) in each type of recovering habitat and reference forest. Afforested areas (A) were characterized by high abundance of herbivorous open-area species of medium body size, high dispersal power,

Table 3 Results of spatial autocorrelation analyses (Moran's I statistics and p) of ground beetle life-history traits in the class of site distances (> 1000 m). Life-history trait

Body size Wing morphology Breeding type Food preference

Distance class 1000 m

Small (< 8 mm) Medium (8-15 mm) Large (> 15 mm) Brachypterous Dimorphic Macropterous Autumn breeders Spring breeders Predators Herbivores

Moran's I

p

−0.078 −0.005 −0.067 −0.197 0.006 −0.09 −0.012 −0.379 0.09 0.397

0.362 0.950 0.472 0.101 0.935 0.286 0.859 0.015 0.281 0.005

and spring breeding cycles. The sites where spontaneous succession occured (SS) were dominated by species whose life traits were similar to those of the assemblages inhabiting the reference forests (mainly predators characteristic of both forest and open habitats, with medium body size, low dispersal power and autumn breeding cycles; Figs. 3 and 4). The reference forests were characterized mainly by large, predatory species, irrespective of dispersal power and breeding cycle (Figs. 3 and 4). The Bonferroni pairwise comparison test of the mean abundance of life traits revealed significant differences between the reference and afforested areas. Comparison of life trait abundances also showed significant differences between the references forest and sites by spontaneous succession, but the mean values were more similar (especially for large, predatory macropterous species, irrespective of breeding type). Life traits characteristic of mature forests (large, brachypterous autumn breeders) were significantly more abundant on areas by spontaneous succession than in afforested sites. Only small and medium-sized species with high dispersal power did not differ significantly between the two types of recovery (Table 4). 4. Discussion Our results indicated that ground beetle life traits are a sensitively indicator of the recovery success, showing replacement of species and adaptation to the habitat created in post-industrial areas. The habitat adaptations of ground beetles strongly depend on the level and intensification of environmental disturbances (Schirmel et al., 2012; Pedley and Dolman, 2014) and thus are useful indicators of habitat recovery (Hodecek et al., 2016; Skalski et al., 2016b). The presence of 5

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Table 4 GLMM results showing the effect of recovery type with sampling transects as a random factor and abundance of ground beetle life history traits. Life-history trait Body size Wing morphology Breeding type Food preference Habitat type

Variable Small (< 8 mm) Medium (8-15 mm) Large (> 15 mm) Brachypterous Dimorphic Macropterous Autumn breeders Spring breeders Predators Herbivores Open areas Forest

Recovery Recovery Recovery Recovery Recovery Recovery Recovery Recovery Recovery Recovery Recovery Recovery

type type type type type type type type type type type type

(Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling (Sampling

larger beetles with low dispersal power, i.e. specialized predators preferring forest habitats, indicates the successful ecosystem recovery, which limits extinction risk (Nolte et al., 2019). These changes also precisely describe the increasing functionality of recovering ecosystems in post-industrial areas (Vandewalle et al., 2010). Species occurring in highly disturbed areas have specific life traits parameters: small body size, high dispersal power, herbivory, and spring development cycles (Ribera et al., 2001; Barbaro and Van Halder, 2009). These adaptations limit the extinction risk of species and characterize many disturbed ecosystems. In each case, small body size and high dispersal capacity allow beetles to escape quickly when a disturbance takes place, as well as to recolonize the area rapidly after the disturbance (Ribera et al., 2001; Gerisch, 2011). It is therefore unsurprising that they have an important role in the early stages of recovery of degraded industrial ecosystems, or that there is a shift towards forest assemblages as succession progresses (Hodecek et al., 2015). Many authors (e.g. Hadčová and Prach, 2003; Laarmann et al., 2015) have shown that plant succession in afforested areas can be unpredictable and differ from natural succession. In some cases

transect) transect) transect) transect) transect) transect) transect) transect) transect) transect) transect) transect)

df

Wald statisctics

p

38 38 38 38 38 38 38 38 38 38 38 38

4.771 226.04 302.63 360.07 55.18 329.23 360.07 396.57 55.18 306.75 323.92 450.70

0.092 0.000 0.000 0.000 0.035 0.000 0.000 0.000 0.035 0.000 0.000 0.000

(Pietrzykowski, 2008; Šebelíková et al., 2016), no significant differences could be seen in total plant species richness between sites afforested via reclamation and spontaneous succession. Our results showed similarities in main vegetation parameters such as canopy closure, tree cover or tree diameter and height between spontaneous succession (SS) and afforestation (A) recovery type. We also should expect similar carabid life trait pattern of habitat specialists. However we observed significantly lower abundance of carabid forest species in afforested areas that might be explained by significantly lower cover of shrub, seedling and herb as well as tree richness (Tables 2, 4). These beetles are usually large carnivores and food and habitat specialists. In our survey, they were significantly affected by afforestation. In contrast, according to Hadčová and Prach (2003), successional processes create more heterogeneous plant communities and thus more varied habitat conditions, which promote greater diversity among potential re-colonizers. This provides a more predictable food source for ground beetles, which promotes specialized species (large body size, low dispersal power and autumn breeding) in landfills where spontaneous succession was observed. NMDS results (Fig. 2) are consistent with findings by Hodecek et al.

Fig. 3. Mean ± SE abundance of carabids according to body size and wing morphology in assemblages of three ecosystem types. Assemblages from particular ecosystem types are designated as follows: A - afforested, SS - spontaneous succession, F - reference forests. Different letters indicate significant differences between recovery procedures (Bonferroni pairwise comparison). 6

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Fig. 4. Mean ± SE abundance of carabids according to food preferences, breeding type and habitat preferences in assemblages of ecosystem types and reference forests. Assemblages from particular ecosystem types are designated as follows: A - afforested, SS - spontaneous succession, F - reference forests. Different letters indicate significant differences between recovery procedures (Bonferroni pairwise comparison).

(2016) and revealed that the landfills where spontaneous succession took place were characterized by highly diverse carabid species composition in comparison to the afforested areas and reference forests. In natural conditions, recovery of a diverse forest ecosystem usually takes about 20–40 years (Dunger et al., 2001; Chazdon, 2008). In our study, this period of time was insufficient for recovery of ground beetle forest communities. The carabid assemblages in afforested areas had a large percentage of species with broad ecological ranges, such as Harpalus rufipes and Calathus erratus, which are often highly dominant in earlysuccessional communities. Many authors have confirmed that environmental disturbances favour mainly herbivorous species with spring breeding cycles, due to limited food resources and a shorter period of potential environmental stress for larvae (Skalski et al., 2015; Bell et al., 2017; Kędzior et al., 2017). As succession of tree stands progresses and habitat conditions stabilize, carabid assemblages should shift into typical forest assemblages (Magura et al., 2001). Our results however, indicated, that in afforested sites, where the forest age was over 20 years, the proportion of forest specialist species was still very low. This is supported by the results of previous studies (Skalski and

Pośpiech, 2006; Skalski et al., 2016b), which showed a very slow recovery rate of beetle assemblages in old reclaimed forest stands. In contrast to technical reclamation (afforestation), natural processes lead to more diverse vegetation cover (Hadčová and Prach, 2003), which is congruent with our results (Table 2). Recovery of plant communities based on the neighbouring species composition creates more heterogeneous systems, that also promotes higher diversity of soil biological elements (Hedde et al., 2012; Hendrychová et al., 2012). Heneberg et al. (2016) has shown that xerothermes formed by sand quarrying subject to spontaneous succession hosted many valuable and rare species compared to reclaimed sites. Our results indicate that the carabid assemblages of landfills where spontaneous succession was observed comprised not only species with broad ecological ranges, but also forest specialists, i.e. predatory species of medium and large body size, with lower dispersal capacity and autumn development cycles. This type of recovery, in which natural processes occur, also promotes many rare and endangered species.

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5. Conclusions

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Based on the findings of this study, analysis of ground beetle life traits seems to be a useful tool for estimating the success of recovery in post-indutrial degraded areas. It can be a sensitive indicator supplementing vegetation structure. This recommendation is applicable in many Central European countries where similar recovery procedures have been common. Life traits such as large body size, low dispersal power, predation and autumn breeding type are characteristic of more successful ecological restoration. The results of this study underline the importance of maintaining ecological restoration of post-industrial areas, including monitoring of restoration success based on the lifehistory traits of ground beetles. From an ecosystem perspective, the use of reclamation procedures consisting only in tree plantation, without restoration of biological elements of the soil, is not conducive to the establishment of good quality ecosystems in post-industrial areas. Declaration of Competing Interest None. Acknowledgments This work was supported by the Polish Ministry of Science and Higher Education and the Personal Scholarschip Fund for academics of Agriculture University in Krakow. The authors like to thank Marek Telk and Agnieszka Losota for technical support and chemical analysis, and Sara Wild for improving the English of the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoleng.2019.105615. References StatSoft, 2012. STATISTICA (data analysis software system), version 12.0. Available from: http://www.statsoft.com/. Barbaro, L., Van Halder, I., 2009. Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes. Ecography. 32, 321–333. https://doi.org/10.1111/j.1600-0587.2008.05546.x. Bell, A.J., Phillips, I.D., Nielsen, S.E., Spence, J.R., 2017. Species traits modify the speciesarea relationship in ground-beetle (Coleoptera: Carabidae) assemblages on islands in a boreal lake. PLoS One 12 (12), e0190174. https://doi.org/10.1371/journal.pone. 0190174. Borges, P.A.V., Hortal, J., 2009. Time, area and isolation: factors driving the diversification of Azorean arthropods. J. Biogeogr. 36, 178–191. https://doi.org/10.1111/j. 1365-2699.2008.01980.x. Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference. Springer, New York. https://doi.org/10.1007/b97636. Chazdon, R.L., 2008. Beyond deforestation: restoring forests and ecosystem services on degraded land. Science. 320, 1458–1460. https://doi.org/10.1126/science.1155365. Dunger, W., Wanner, M., Hauser, H., Hohberg, K., Schulz, H.J., Schwalbe, T., 2001. Development of soil fauna at mine sites during 46 years after afforestation. Pedobiologia. 45, 243–271. https://doi.org/10.1078/00314050122254957. Frouz, J., Ellhotová, D., Kuraz, V., Sourkova, M., 2006. Effects of soil macrofauna on other soil biota and soil formation in reclaimed and unreclaimed post mining sites: results of a field microcosm experiment. Appl. Soil Ecol. 33, 308–320. https://doi.org/10. 1016/j.apsoil.2005.11.001. Frouz, J.K., Prach, V., Pižl, L., Háněl, J., Starý, K., Tajovský, J., Materna, V., Balík, J., Kalcík, J., Řehounková, K., 2008. Interactions between soil development, vegetation and soil fauna during spontaneous succession in post mining sites. Eur. J. Soil Biol. 44, 109–121. https://doi.org/10.1016/j.ejsobi.2007.09.002. Gerisch, M., 2011. Habitat disturbance and hydrological parameters determine the body size and reproductive strategy of alluvial ground beetles. Zookeys. 100, 353–370. https://doi.org/10.3897/zookeys.100.1427. Graf, E.D., 1969. Compaction grouting technique and observations. J. Soil. Mech. Found. Divi. 95 (5), 1151–1158. Hadčová, D., Prach, K., 2003. Spoil heaps from brown coal mining: technical reclamation versus spontaneous revegetation. Restor. Ecol. 11, 385–391. https://doi.org/10. 1046/j.1526-100X.2003.00202.x. Haigh, M.J., 2000. The aims of land reclamation. In: Haigh, M.J. (Ed.), Reclaimed Land. Erosion Control, Soils and Ecology. AA. Balkema, Rotterdam, the Netherlands, pp. 1–20. Hammer, Ø., Harper, D.A.T., Paul, D.R., 2001. Past: paleontological statistics software

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