Post-industrial areas as successional habitats: Long-term changes of functional diversity in beetle communities

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Post-industrial areas as successional habitats: Long-term changes of functional diversity in beetle communities Jiri Hodeceka,∗ , Tomas Kurasc , Jan Siposa,b , Ales Dolnya a Dep. of Biology and Ecology/Institute of Environmental Technologies, Faculty of Science, Univ. of Ostrava, Chittussiho 10, 710 00, Ostrava, Czech Republic b Dep. of Vegetation Ecology, Institute of Botany, Academy of Sciences of the Czech Republic, Lidicka 25/27, 602 00, Brno, Czech Republic c Dep. of Ecology and Environmental Sciences, Faculty of Science, Palacky Univ. in Olomouc, Tr. Svobody 26, 771 46, Olomouc, Czech Republic

Received 4 September 2014; accepted 23 June 2015

Abstract Understanding succession is one of the main goals in ecosystem ecology, but very few studies regarding arthropods have actually examined this topic in sufficient detail. Missing are studies that examine the long-term trend of primary succession of arthropods in post-industrial habitats and also the functional consequences of primary succession on arthropods. We used epigeic beetles as a model group to investigate the process of primary succession of arthropods on spoil heaps for about 30 years of spontaneous development. For carabid beetles, we calculated indices of functional diversity (functional evenness, functional richness and functional divergence). To quantify functional diversity we used these functional traits: wing morphology, habitat preference and humidity dependence. Our results reveal that the main environmental factor determining the structure of beetle communities is spoil heap age, which is itself correlated with forest cover. The descriptive rank-abundance models that best fit our community structure were Gambin and Zipf – Mandelbrot. Abundances of brachypterous and forest species were positively correlated with successional age. Our results provide evidence that primary succession in post-industrial habitats differs from that in more natural habitats due to the rapid rate of successional changes and their attributes. In particular, abiotic factors are constitutive in comparison to interspecific competition during succession. The canonical correspondence analysis model identified that irregular disturbances are another important phenomenon of succession in post-industrial habitats. We assume that constant indices of functional evenness and richness reflect rapid colonization from surrounding habitats. Functional divergence was significantly correlated with increasing proportion of forest species.

Zusammenfassung Sukzessionen zu verstehen ist eines der Hauptziele der Ökosystemökologie, aber nur wenige Untersuchungen an Arthropoden haben dieses Thema tatsächlich mit genügender Genauigkeit betrachtet. Es fehlen Untersuchungen, die den langfristigen Trend der Primärsukzession bei Arthropoden in Industriefolgehabitaten und die funktionalen Konsequenzen der Primärsukzession für Arthropoden erforschen. Wir wählten epigäische Käfer als Modellgruppe, um die Primärsukzession von Arthropoden auf

∗ Corresponding

author. Tel.: +420 777621346. E-mail address: [email protected] (J. Hodecek).

http://dx.doi.org/10.1016/j.baae.2015.06.004 1439-1791/© 2015 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

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Abraumhalden über 30 Jahre spontaner Entwicklung hinweg zu untersuchen. Für die Laufkäfer kalkulierten wir Indizes der funktionalen Diversität (funktionale Evenness, funktionaler Reichtum und funktionale Divergenz), wobei wir die folgenden funktionalen Merkmale benutzten: Flügelmorphologie, Habitatpräferenz und Feuchteabhängigkeit. Unsere Ergebnisse zeigten, dass das Alter der Abraumhalde der wichtigste die Struktur der Käfergemeinschaft bestimmende Umweltfaktor war, wobei das Alter mit der Waldbedeckung korreliert ist. Die deskriptiven Rang-Abundanz-Modelle, die die Gemeinschaftsstruktur am besten beschrieben, waren Gambin und Zipf-Mandelbrot. Die Abundanzen der kurzflügeligen Arten und der Waldarten waren positiv mit dem Sukzessionsalter korreliert. Unsere Ergebnisse belegen, dass sich die Primärsukzession in Industriefolgehabitaten von der in naturnäheren Habitaten unterscheidet, was auf die Geschwindigkeit der Sukzessionsänderungen und ihrer Merkmale zurückgeht. Insbesondere sind abiotische Faktoren bestimmend im Vergleich zu interspezifischer Konkurrenz während der Sukzession. Eine kanonische Korrespondenzanalyse zeigte, dass unregelmäßige Störungen ein weiteres wichtiges Phänomen bei der Sukzession in Industriefolgehabitaten ist. Wir nehmen an, dass konstante Werte von funktionaler Evenness und funktionalem Reichtum die schnelle Besiedelung aus Habitaten in der Umgebung widerspiegelt. Die funktionale Divergenz war signifikant mit der Zunahme von Waldarten korreliert. © 2015 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

Keywords: Carabids; Environmental factors; Functional traits; Landscape restoration; Rank-abundance models; Species turnover; Spoil heaps

Introduction The replacement of species in an environment over time is typical for ecosystem development. Successional processes are traditionally divided into primary and secondary successions (Miles, 1979). Primary succession is ecosystem development in situations where no previously developed soil exists. Species which de novo colonize this environment create and modify it by their presence (Dobson, Bradshaw, & Baker, 1997; Vitousek, Matson, & Cleve, 1989). Unlike cases of secondary successions, in the initial stages of primary successions random processes are of significant importance and species change is determined mainly by abiotic environmental factors (Majer, 1989; Walker & Moral, 2003). Urbanized areas today cover approximately 1 – 6% of land (Alberti et al., 2003), and more than 50% of people live in them (Millennium Ecosystem Assessment, 2005). Some urbanized and post-industrial locations present examples of new primary successional habitats. The spoil heaps are such unique anthropic ecosystems, since they lack a soil profile with diaspores and have specific microclimate (Ash, Gemmell, & Bradshaw, 1994; Majer, 1989). Urban and post-industrial ecosystems can become a refuge for species and can increase the biological richness of cultural landscape (Tropek et al., 2010). That makes them among the most important ecosystems on Earth. Moreover, various mining activities have affected about 1% of the Earth’s terrestrial surface and occur in most countries of the world (Walker, 2012). Therefore, there are increasing numbers of studies highlighting the succession of post-industrial habitats, including in the context of restoration ecology and conservation biology (Harabis, Tichanek, & Tropek, 2013; Lundholm & Richardson, 2010; Walker & Moral, 2003). The most common studies focusing on organisms colonizing such places relate to vegetation (Ash et al., 1994; Kovar, 2004; Prach et al., 2013; Song, Shu, Wang, & Liu, 2014). There are several papers focusing on primary succession of arthropods in post-industrial habitats,

however, they focus mainly on specific topics e.g. importance of the survival of endangered species (Tropek et al., 2010; Tropek, Cerna, Straka, Cizek, & Konvicka, 2013) or changes of species diversity in time (Schwerk & Szyszko, 2011; Schwerk, 2014). Long-term trends in arthropod succession and studies based on functional diversity (FD) are missing entirely, although arthropods can often indicate changes in an environment in a more comprehensive and sensitive manner than changes on a vegetation or vertebrate level (Gerlach, Samways, & Pryke, 2013; Hodkinson, Webb, & Coulson, 2002; Kremen et al., 1993; Samways, McGeoch, & New, 2010). During primary succession, species associated with newly created habitats (pioneer species) will increase in number over time as a result of colonization processes. The colonization of new habitats is determined mainly by (a) accumulation of resources, (b) species pool, (c) edge effect and (d) the species – area relationship (MacArthur & Wilson, 1967; Walker & Moral, 2003). Such effects determining the structure of temperate ecosystems can be expected in forest species. These species will respond to an alteration in the environment during primary successional seres by increased abundance and species richness. Species which are not associated with forest habitats show the opposite trend. Such trends are usually documented in terms of species diversity (Stenbacka, Hjältén, Hilszcza´nski, & Dynesius, 2010). However, guilds or functional groups of arthropods can respond to the availability of specific resources and environmental factors, which may change in the course of succession. Functional roles may thus be a key factor in diversity responses to habitat succession (Gibb, Johansson, Stenbacka, & Hjältén, 2013). FD provides a new concept for the interpretation of successional changes. Alteration of vegetation structure over time determines distribution of animals in time and space and their life-history traits (Lytle & Poff, 2004, Renöfält, Nilsson & Jansson 2005). Functional characteristics of organisms contribute to fitness, because functional characteristics

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determine their survival (Violle et al., 2007). The main advantage of using FD is to describe the relationships in between organisms and changes in their environment (Díaz & Cabido, 2001; Tilman, 2000). Species diversity does not fully reflect these relationships. In contrast to traditional measures used to describe community development (species richness, diversity and abundance), the use of FD is still rare, even though FD strongly determines ecosystem functioning (Díaz & Cabido, 2001; Walker & Moral, 2003). There are only a few published papers focusing on succession which are based on the FD of arthropods (Taillefer & Wheeler, 2012; Gerisch, Agostinelli, Henle, & Dziock, 2012; Gibb et al., 2013; Gerisch, 2014). Species abundance distributions (SAD) shows how species abundances are distributed within ecological communities (McGill et al., 2007; Tokeshi, 1993). This method could reveal patterns in rarity and commonness of the species. SAD models are either based on mathematical (Zipf – Mandelbrot, Gambin) or biological (niche partitioning models, broken stick models and pre-emption model) principles (Matthews et al., 2014). SAD models can be used to analyse changes of community structure during succession (Bazzaz, 1975) and to measure the effects of disturbances on the communities (Gray & Mirza, 1979). They are an important approach which can be used also in macro-ecological concepts as neutral theory or niche theory (Hubbell, 2001; Matthews et al., 2014). Niche theory assumes that species traits are evolutionary adaptations to particular environments (Hutchinson, 1957). Neutral theory assumes that all species are functionally equivalent and species assemblages are formed by stochastic drift (Hubbell, 2001). We hypothesized that models which are not attributed to niche partitioning would provide a better match to our data. This would mean that abiotic factors determined community structure. In the present paper, we present the process of arthropod succession on black coal spoil heaps during approximately 30 years of spontaneous development, focusing on an analysis of arthropod structure and FD in a gradient of primary succession. Based on the characteristics of the spoil heap environment we can expect that changes in the community structure will be determined mainly by vegetation. In early successional seres mainly generalists with high dispersal ability and a preference for open habitats (pioneer species) will be present. In late successional seres the specialists and better competitors (forest species) should dominate. Due to random colonization in the initial phases of succession the species abundances will be unevenly distributed. Therefore we assumed that the species composition will be determined by the environmental conditions in the sense of “habitat templet theory” (Southwood, 1977, 1988). We can also expect an important role of edge effect because of the relatively small areas of the spoil heaps, which is in concordance with the island biogeogeography theory (MacArthur & Wilson, 1967). In early successional seres the FD will be mainly influenced by immigration of species from surrounding habitats, on the other hand in late phases of succession functional characteristics of the species will be determined mainly by

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vegetation cover. A specific feature of post-industrial areas can be irregular disturbances (Harabis et al., 2013), which can increase species diversity and FD in late phases of succession (intermediate disturbance theory). Therefore we hypothesized (i) that the gradual development of a spoil heap ecosystem would cause the replacement of generalists associated with open habitats by forest species; (ii) irregular disturbances will be an important factor in determining communities of post-industrial areas. Our aim was to discover what determines these changes and how rapid the changes are.

Materials and methods Study area The study was conducted in the north-eastern part of Czech Republic in the Upper Silesian industrial region, the largest conurbation in central Europe. Deep underground mining has been going on here since the 1850s. The area is characterized by intense devastation of many landscape elements, caused mainly by black coal mining and iron metallurgy. Underground mining has contributed to many changes in the lithosphere, hydrosphere, atmosphere, biosphere and soil cover. The anthropogenic landforms can generally be divided into landscape alterations consciously created by humans (spoil heaps, tailings and slurry lagoons) and changes originating as unintentional consequences of human activities (subsidence) (Dolny & Harabis, 2012). The study took place on three spoil heaps (Ema, Bezruc and Zarubek) in the city of Ostrava. These spoil heaps had been created by accumulating spoil after deep underground mining of black coal. Spoil depositing was ended at the turn of the 1950s to the 1960s. During succession, the spoil heaps were spontaneously colonized by pioneer species of plants and woody species. Among the most dominant trees residing on the spoil heaps today are such species as Populus x canadensis, Betula pendula and Fraxinus excelsior (Sobotkova, 1995). The Zarubek spoil heap (49◦ 49 40.8 N 18◦ 17 56.0 E, 224 m a.s.l.) was begun in the 1940s. Zarubek spans an area of 6.3 ha and its elevation above the surrounding terrain is about 7 m. The Ema spoil heap (49◦ 50 23.5 N 18◦ 18 53.2 E, 323 m a.s.l.) was started around 1920, and together with the Bezruc spoil heap it creates a complex area of 20 ha. The elevation above the surrounding terrain is about 80 m. The Bezruc spoil heap (49◦ 50 29.5 N 18◦ 18 49.6 E, 305 m a.s.l.) was begun in 1920 and its elevation above the surrounding terrain is up to 60 m.

Study group and sampling As a model group of arthropods, we chose epigeic beetles because they represent a very abundant and diverse

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taxonomical group with important ecological functions in the ecosystem (Gerisch et al., 2012; Gerisch, 2014; Krooss & Schaefer, 1998; Schulze et al., 2004). To analyse these species, we used a canonical correspondence analysis (CCA) model and rank-abundance models. The ordination methods allow us to test which biotic and physical factors determine arthropod communities. Rank-abundance distributions can be used to describe the structure of the communities. We tested the rank-abundance distributions found against theoretical niche-based and mathematical models. To test changes of functional groups of beetles and FD, we chose the family Carabidae. Carabids are effective indicators in the ground layer because they are sensitive to landscape changes with a large range of responses, and their taxonomy and ecology are well-known (Gerlach et al., 2013; Rainio & Niemelä, 2003). We used pitfall traps to capture beetles. Each trap was made of a 0.3 l plastic cup. The pitfall traps were covered with small tin roofs and filled with a 2 – 4% formaldehyde solution. Material was collected during 1975 – 1976 (8 pitfall traps on each of the Zarubek and Bezruc spoil heaps), 1993–1995 (5 pitfall traps on each of the three spoil heaps), and 2006 – 2007 (5 pitfall traps on each of the three spoil heaps, as in the previous period). In total we had data from 7 years (1975, 1976, 1993, 1994, 1995, 2006 and 2007). The number of traps was chosen due to the relatively small areas of the spoil heaps. Analysis of similarities (ANOSIM) results indicated that species captured within each spoil heap were highly mixed among traps (for Zarubek R: −0.009; for Ema R: 0.041 and for Bezruc R: 0.094). The value of the R parameter close to 0 indicates no differences between the traps. Therefore we assumed that the number of traps was sufficient for the sampling of the spoil heap habitats. Because of the different numbers of pitfall traps on the Zarubek and Bezruc spoil heaps in the 1970s, the data was standardized by dividing the species abundance by the number of traps in the particular year. The traps were visited approximately every 14 days.

Data arrangement The following explanatory variables were used for the CCA model: (a) forest cover, (b) herb cover, (c) bare ground cover and (d) spoil heap age. Forest, herb and bare ground cover were coded as continuous variables. Vegetation cover was recorded for an area with a radius of 50 m around the pitfall trap. This distance defines the habitat of a spoil heap (including its nearest surroundings) and also covers the dispersal ability of most epigeic beetles (Niemelä, 2001 Riecken & Raths, 1996). Habitat areas were calculated using ArcGIS Desktop (ArcView) v10. Spoil heap age was individually coded for each year of sampling. This factor was calculated as the number of years that had passed since spoil depositing had ceased. This corresponds to the gradual changes in the insect and plant communities over time. Each spoil heap was

coded as a categorical variable and was used as a co-variable in the CCA model. Species data for the CCA model were coded as the number of individuals in a particular sampling year within each spoil heap. Based on the literature, we chose the following species traits of carabids to be used for calculating FD: wing morphology, habitat preference and humidity dependence (see Appendix A). These traits are of great importance to understanding of how species change during succession. Wing morphology of ground beetles is important for dispersal and recolonization ability (Gerisch et al., 2012; Gerisch, 2014). Each species was assigned to one of the following categories: macropterous (winged), brachypterous (wingless) and dimorphic (both forms can appear within a species) (Hurka, 1996; Stanovsky & Pulpan, 2006). For habitat preference, we divided the species into forest species, species of open habitats and generalists (Hurka, 1996; Lindroth, 1992; Stanovsky & Pulpan, 2006). Humidity dependence was evaluated only for species for which this strategy is relevant, i.e. hygrophiles and xerophiles (Stanovsky & Pulpan, 2006). These traits can serve as proxies for less mobile species associated with more humid forest habitats and on the other hand they can determine highly mobile species associated with open habitats with a xerothermic character.

Data analysis We used a unimodal direct gradient analysis (i.e. CCA) to test the effects of the environmental variables on epigeic beetle abundances (ter Braak & Smilauer, 2002). Areas of bare ground cover, herb cover and forest cover as well as spoil heap age were considered as explanatory variables. Each spoil heap was used as a co-variable in the CCA model to eliminate variability caused by the distinctive characteristics of the particular spoil heap. Forward selection was used to select the significant explanatory variables. We configured the CCA model with axis scaling by inter-species distances. Species abundances were transformed using the logarithm function and standardized by the number of traps on each spoil heap and year. Rare species were down-weighted. The significance of the canonical axis and explanatory variables were tested by Monte-Carlo permutation test (5000 permutations restricted by co-variables). Indices of FD were chosen based on recent literature (Leps, Bello, Lavore, & Berman, 2006; Mason, Mouillot, Lee, & Wilson, 2005). As a basic feature, we calculated functionally unique species for each successional year, computed as the number of species sharing a unique combination of functional characteristics. As components of FD, we computed: (a) functional richness, which indicates the width of a niche space filled with species; (b) functional evenness, indicating the degree of evenness of species abundance distribution in a niche space and (c) functional divergence, which indicates how the species abundance distribution influences

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the divergence of a functional characteristic in a niche space (Mason et al., 2005). Rank-abundance models were used for visualizing species abundance distribution during successional events on a particular spoil heap. Rank-abundance models were fitted by the maximum likelihood method. Niche-oriented (pre-emption and broken stick) and descriptive (log-normal, Zipf, Zipf – Mandelbrot and Gambin) models were used to model species distribution data. We used the most commonly used rank – abundance models (see Magurran, 1988; Tokeshi, 1993): (a) log-normal, Zipf and Zipf – Mandelbrot which are generalized linear models with logarithmic link function, (b) Gambin which also fits as generalized linear model combining the gamma distribution with binomial sampling method (estimating the parameter alpha, which determines the shape of the gamma distribution), (c) niche pre-emption model, which is fitted as purely non-linear model and (d) broken stick which fits as log-linear model. The model with the lowest Akaike information criterion (AIC) was chosen as the one fitting best the species abundance distribution on the particular spoil heap and year. We utilised the Vegan package in R 3.0.1. (R Development Core Team, 2013) for species rank – abundance modelling. The relationship between the species richness of a particular functional group or FD as response variables and the age of the spoil heaps was examined using a generalized linear model with Gaussian error distribution and log link function. Standard errors were corrected using quasi-likelihood function. For the degree of functionally unique species, we built the model assuming Poisson error distribution. The effect of each explanatory variable was tested also for its significance of the quadratic transformation. Step-wise selection based on the lowest AIC was used to choose the best transformation function of the explanatory variable. We used an F-test to determine the significance of each variable because it is a robust test for overdispersed data. The relationship between the alpha parameter and the spoil heap age was fitted by generalized linear model with Gamma error distribution and inverse link function. The significance effect of spoil heap age on alpha parameter was tested by χ2 statistic. Data were analysed using R software (R Development Core Team, 2013) and Canoco 4.5 (ter Braak & Smilauer, 2002).

Results Species composition and rank – abundances A total of 16,469 epigeic beetle individuals belonging to 303 species and 31 families were recorded during the sampling periods (see Appendix A). The most dominant families were Leiodidae (42.6%) and Staphylinidae (33.0%), then Carabidae (10.1%), Curculionidae (5.0%) and Cryptophagidae (4.4%). Among the regionally rare species, there were recorded a species from the family

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Table 1. Rank – abundance models of epigeic beetle communities by spoil heap and year. Spoil heap/year

AIC

Alpha

Best fitted model

Bezruc/1975 Bezruc/1976 Bezruc/1993 Bezruc/1994 Bezruc/1995 Bezruc/2006 Bezruc/2007 Ema/1993 Ema/1994 Ema/1995 Ema/2006 Ema/2007 Zarubek/1975 Zarubek/1976 Zarubek/1993 Zarubek/1994 Zarubek/1995 Zarubek/2006 Zarubek/2007

377 410 75 171 158 162 144 111 113 136 100 110 324 333 108 148 133 128 133

0.7771 1.076 0.782 0.9566 0.9536 0.9224 1.78 1.233 1.196 1.192 1.146 0.7049 0.8708 0.8806 0.4505 0.534 0.6159 0.4834 0.6091

Gambin Gambin Gambin Zipf – Mandelbrot Zipf – Mandelbrot Zipf – Mandelbrot Zipf – Mandelbrot Gambin Zipf – Mandelbrot Zipf – Mandelbrot Zipf – Mandelbrot Zipf – Mandelbrot Gambin Gambin Gambin Gambin Gambin Gambin Gambin

Leiodidae, Choleva paskoviensis; the rare forest carabids Abax schueppeli rendschmidti and Leistus rufomarginatus; the xerotherm rove beetles Tasgius pedator pedator and Astrapeus ulmi; and other rare species of the Staphylinidae family, Medon castaneus, Ocypus compressus, Ilyobates nigricolis, Parocyusa rubicunda and Platydracus latebricola. Descriptive models fit the abundance distribution of the beetle assemblages better than the niche-oriented models for all years and all spoil heaps did. Gambin and Zipf – Mandelbot were the descriptive models which best explained our data (see Appendix A and Table 1). The alpha parameter significantly decreased during succession on the spoil heaps Zarubek (y = −0.0111x + 22.792; R2 = 0.6577; p = 0.001) and Ema (y = −0.0236x + 48.279; R2 = 0.5473; p = 0.04).

Spoil heap features and their effects on beetle communities The effects of environmental variables were studied by CCA model. After removing the variability defined by covariables, the model explained 47.2% of the variability in species data (Table 2). Spoil heap age was the factor which explained the most variability (Table 3). The effect of the vegetation variables and spoil heap age were all significant (Table 3). Spoil heap age, which represented more than 30 years of succession, correlated most with the first axis (Fig. 1). Another factor which correlated with the first axis was herb cover (Fig. 1). The species which correlated with the forest cover variable showed the opposite trend (Fig. 1). Bare

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Table 2. Results of the canonical correspondence analysis model of beetle abundances and environmental factors on spoil heaps. Axes

I.

Eigenvalues Species – environment correlations Cumulative percentage variance of species data of species – environment relation Sum of all eigenvalues Sum of all canonical eigenvalues Test of significance of first canonical axis Test of significance of all canonical axes

II.

0.520 0.999 20.8 44.2 2.492 1.175 F-ratio = 3.161 F-ratio = 2.678

0.287 0.980 32.4 68.6

III. 0.194 0.959 40.1 85.1

IV. 0.175 0.980 47.2 100.0

P-value = 0.0002 P-value = 0.0002

ground cover correlated with the second axis (Fig. 1). The abundance of forest species (e.g., Carabus hortensis, Leistus rufomarginatus and Astrapaeus ulmi) grew with increasing forest cover. On the other hand, decreases in herb cover negatively affected such species as Catops nigricans, Agrypnus murinus and Xantholinus linearis.

Changes in functional traits of ground beetles over time The richness of brachypterous species was positively correlated with time (F1,17 = 2.42, p = 0.13) while macropterous species showed a negative correlation (F1,17 = 3.05, p = 0.05) (Fig. 2A). Dimorphic species showed an invariant trend during the whole succession. Forest species richness was positively correlated with time (F1,17 = 3.32, p = 0.05), whereas the species of open habitats showed the opposite trend (F1,17 = 0.95, p = 0.34) (Fig. 2B). During succession, the richness of hygrophiles also increased (F2,16 = 0.19, p = 0.83) (Fig. 2C). In contrast, the number of xerophiles decreased over time (F1,17 = 0.76, p = 0.39) (Fig. 2C). However, only trends of macropterous and forest species were significant. The number of functionally unique species decreased with sampling year (Fig. 3). Functional evenness showed no significant dependence on successional age (F1,17 = 0.001, P = 0.97) (Fig. 4A). Although the index of functional richness decreased slightly with time, this decrease was not significant (F1,17 = 0.939, P = 0.34) (Fig. 4B). The index of functional divergence grew linearly, and the increase was significant (F1,17 = 6.35, P = 0.02) (Fig. 4C).

Table 3. Forward selection results of the canonical correspondence analysis for parameters of individual spoil heaps. Environmental variable

Variability explained

p

F

Spoil heap age Bare ground Forest cover Herb cover

0.48 0.27 0.23 0.20

0.000 0.000 0.001 0.030

3.59 2.18 1.97 1.77

Fig. 1. Canonical correspondence analysis of beetles and environmental factors on spoil heaps. Species with weight >10% are displayed. Each species name is given in acronyms, as follows: AgrMur—Agrypnus murinus, AleBre—Aleochara brevipennis, AleFun—Aleochara funebris, AmaPra—Amara praetermissa, AntAtr—Anthobium atrocephalum, AstUlm—Astrapaeus ulmi, BarPel—Barypeithes pellucidus, CalErr—Calathus erratus, CarHor—Carabus hortensis, CarCon—Carabus convexus, CarCor—Carabus coriaceus, CarVio—Carabus violaceus, CatNig—Catops nigricans, CorObs—Cordalia obscura, CryPal—CryLyp—Cryptophagus lycoperdi, Cryptophagus pallidus, CryPun—Cryptophagus punctipennis, DruCan—Drusilla canaliculata, EusLon—Eusphalerum longipenne, FalTho—Falagria thoracica, LagHir—Lagria hirta, LeiFer—Leistus ferrugineus, LeiRuf—Leistus rufomarginatus, NarVel—Nargus velox, OmaRiv—Omalium rivulare, OtiOva—Otiorhynchus ovatus, OtiSin—Otiorhynchus singularis, ParRub—Parocyusa rubicunda, PoeCup—Poecilus cupreus, PteNig—Pterostichus niger, PteObl—Pterostichus oblongopunctatus, PtoSer—Ptomaphagus sericatus, SepTes—Sepedophilus testaceus, SciFum—Sciodrepoides fumatus, SciWat—Sciodrepoides watsoni, TasPed—Tasgius pedator, TriDer—Trixagus dermestoides, XanLin—Xantholinus linearis. Photo by Jiri Hodecek.

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Functionally unique species

25

7

y = -0.2086x + 427.05 R² = 0.222

20 15 10 5 0 1970

1980

1990

2000

2010

Years Fig. 3. Changes in abundances of functionally unique ground beetle species during succession on spoil heaps. Functionally unique species are represented by the number of species sharing a unique combination of functional characteristics. Each point represents data from one spoil heap in one year.

Discussion Changes in communities over time and main environmental factors

Fig. 2. Changes in functional traits of ground beetles during succession on spoil heaps. The species richness was calculated as number of species of each trait category divided by the sum of all species in each year. The lines were fitted by the least sum of squares. The significant trends are displayed by full lines. Each point represents data from all spoil heaps in particular year. (A) Trends in species richness of wing morphology categories, (B) Trends in species richness of habitat preference categories, (C) Trends in species richness of humidity dependence categories.

Communities of terrestrial arthropods are changing significantly during primary succession. Our results suggest that the main factor which determines the structure of beetle communities is spoil heap age, which is itself positively correlated with increasing tree cover over time. The initial stage of primary succession was represented by an environment without vegetation and which developed over time into a habitat with herb cover and later with forest cover. In principle, our results correspond with changes in communities of arthropods in secondary successional habitats (e.g., Koivula, Kukkonen, & Niemelä, 2002; Scheu & Schulz, 1996). The first axis of our CCA model can be explained by spoil heap age as the main gradient in species data. Forest species positively correlated with the first axis, whereas those species associated with herb cover correlated with it negatively. This trend supports the universal conception of community development in which initial successional seres are successfully colonized mainly by species associated with habitats having sparse vegetation (Hodkinson et al., 2002). However, bare ground habitat did not correlate with time (i.e. the first axis). We explain this phenomenon by irregular disturbances of vegetation cover which can be caused by restoration activities or urbanization of the spoil heaps’ surroundings (Harabis et al., 2013). In contrast to large disturbances which can completely destroy all communities (Cooke & Johnson, 2002; Dornelas, Soykan, & Ugland, 2010), small disturbances may enhance species richness by releasing resources and promoting the coexistence of species adapted to different conditions (Connell, 1978; Holt, 2008). Thus, disturbance – succession dynamics create highly heterogeneous, patchy conditions, which may generate resources for rich arrays of species (Cizek, Vrba, Benes, Hrazsky, & Koptik, 2013). Similar disturbance processes can be found also at other industrial sites,

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Functional evenness

(A) 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 1970

R² = 6E-05

1980

1990

2000

2010

Years

Functional richness

(B) 0.5 0.45 0.4 0.35 0.3 0.25 0.2 0.15 0.1 0.05 0 1970

R² = 0.0463

1980

1990

2000

2010

Years

Functional divergence

(C)

R² = 0.277

1.2 1 0.8 0.6 0.4 0.2 0 1970

1980

1990

2000

2010

Years Fig. 4. Changes in FD indices of ground beetles during succession on spoil heaps. Each point represents data from one spoil heap in one year. The lines were fitted by the least sum of squares. The significant trends are displayed by full lines. (A) Trend of functional evenness during succession, (B) Trend of functional richness during succession, (C) Trend of functional divergence during succession.

The rank – abundance models show Gambin and Zipf – Mandelbrot to be those distribution models that best fit our beetle communities. Frontier (1985) interpreted Zipf – Mandelbrot as a model, which reflects a process where the colonists of late successional seres are habitat specialists. The Gambin model estimates the alpha parameter, which reflects a complexity of processes structuring a community (Ugland et al., 2007). Many studies have proven that species abundance distributions take on a log-normal character during later stages of succession (Bazzaz, 1975; McGill et al., 2007). By contrast, our results displayed no trend in species abundance distribution during succession. Compare to the niche-oriented models, we found that the descriptive models were more appropriate for fitting beetle abundance distributions. We therefore assume that abiotic factors played an important role in structuring beetle communities during all successional seres. These results are also confirmed by studies of pollution impact to benthic communities. It was found that in highly disturbed communities life-history strategies are less important than effects of environmental conditions (Gray et al., 1990; Ugland et al., 2008). In their studies the disturbance influenced species diversity as well as the species abundance distribution. It has also been recognized that disturbed communities often differ from lognormal distribution, if the disturbance is not persistent (Gray, 1981). With disturbance intensity the abundance of generalists increased, which is similar to early phases of succession on post-industrial areas (Gray et al., 1990; Ugland et al., 2008). The decreasing trend of the alpha parameter on the spoil heaps Ema and Zarubek reveals that during succession the number of factors which determined the structure of the communities decreased. We explain that by the increase of forest cover during succession, which unifies the biotic and physical conditions of the spoil heaps. The forest cover should select specialists for this type of habitat. This is supported by the rank-abundance model (Zipf – Mandelbrot) as well as the CCA model. No community was fit by the niche-oriented models, which determine community structures based rather on interspecific interactions (McGill et al., 2007; Tokeshi, 1993). Therefore, at disturbed sites, competition does not have to increase during succession, because fluctuating abiotic factors (Gerisch et al., 2012; Gibb et al., 2013) together with the dispersal of the species from the surrounding area (Harpole & Tilman, 2006; Niemelä, Haila, & Punttila, 1996) will play crucial roles. Moreover, irregular disturbances which affect species abundances can also decrease the effect of competition on the structure of communities (Grime, 1979).

Changes in functional groups over time either terrestrial (Tropek et al., 2010, 2013) or even aquatic (Dolny & Harabis, 2012; Gray, Clarke, Warwick, & Hobbs, 1990; Ugland, Bjørgesæter, Bakke, Fredheim, & Gray, 2008). Irregular disturbances may thus be an important phenomenon of primary successional changes at post-industrial sites.

Initial stages of succession are characterized by the presence of pioneer or, more precisely, r-strategists, which are functionally uniform (Pianka, 1970). Our study did not confirm this common trend of low FD at the beginning of

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succession. In early successional stages, we identified an increased number of species with unique combinations of functional characteristics. This could be explained by the relatively small sizes of the studied spoil heaps and their accessibility to a broader spectrum of functionally different species from surrounding areas. The spoil heaps are also located in an urban area, a location type having relatively high heterogeneity of habitats (Ferenc et al., 2014) and microclimatic conditions (Peters & McFadden, 2010). For the studied region, this phenomenon has been described by Havrlant (1980) and Sobotkova (1995). Therefore, species with similar combinations of functional traits are selected by unification of vegetation cover over time (Boer, 1970; Madej & Stodołka, 2008). The uniformity of forest habitats selects species of similar functional traits, and hence FD will diminish (Boer, 1970; Niemelä, 2001; Silva, Aguiara, Niemelä, Sousac, & Serranoa, 2008). Moreover, functional evenness can be determined by the specific character of spoil heaps. We discovered a constant index of functional evenness, which differs from the traditional conception of community development during succession wherein functional evenness grows with increasing abundance of species having different ecological functions (Magurran, 1988; Tokeshi, 1993). Since the species pool of the Ostrava conurbation is relatively low (Stanovsky & Pulpan, 2006), functional evenness does not change significantly. Another attribute is the relatively small area of the spoil heaps, which corresponds to an enhanced edge effect (Donovan, Jones, Annand, & Thompson, 1997; MacArthur & Wilson, 1967; Murcia, 1995; Magura, 2002). Therefore, species abundances on spoil heaps are similar to those in the surrounding habitats and functional evenness remains constant. Linkage of biota with spoil heap surroundings can be considered as another typical phenomenon for primary successions at post-industrial sites. The index of functional richness – meaning the occupancy of niche space in the community – showed a similar trend. Its value decreased slightly but not significantly during succession because the succession did not reach the mature stage. We assumed gradual overgrowing by trees on spoil heaps, despite the effect of irregular anthropogenic disturbances of vegetation cover during succession. Similarly to Gerisch et al. (2012), we identified a rising index of functional divergence. Functional divergence grew with increasing forest cover on spoil heaps (i.e. with lower fluctuation of microclimatic conditions and greater unification of vegetation) (Koivula, 2002). We explain this by the gradual increase of more specialized species (e.g., Koivula et al., 2002; Silva et al., 2008). Early successional seres mainly supported species of open habitats (e.g., Calathus erratus, Amara aenea, Synuchus vivalis) and macropterous species (e.g., Amara praetermissa, Platynus assimilis, Pterostichus oblongopunctatus), whereas in later successional seres the abundance of forest species (e.g., Carabus hortensis, Leistus rufomarginatus, Abax schueppeli rendschmidti) and brachypterous species (e.g., Carabus convexus,

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Carabus hortensis, Abax schueppeli rendschmidti) increased. A similar trend is seen in the decrease of xerophiles (e.g., Licinus depressus, Ophonus melleti, Panagaeus bipustulatus), which were rather replaced by hygrophiles (e.g., Notiophilus palustris, Pterostichus strenuus). The low functional divergence in the initial stages of succession indicates that, although FD was high from the beginning, most species used similar life-history strategies, allowing them to quickly colonize the spoil heaps and survive the extreme conditions.

Conclusions In this study, we described how the structure of epigeic beetle communities changes during primary succession on spoil heaps. Our results suggest that primary successions in post-industrial habitats differ from primary successions in more natural habitats by their rate of successional changes and their attributes. Descriptive models indicate that communities during succession at post-industrial sites are affected mainly by abiotic environmental factors and not by the competition that is typical for more natural habitats. Due to the relatively small areas of the spoil heaps and to edge effects, we assume that the species pool of the surrounding habitats and quick colonization were of great importance. This corresponds to the invariant indices of functional evenness and functional richness. The significant increase of functional divergence indicates that the proportion of abundances in functional groups of forest specialists rises during succession at post-industrial sites. We further identified a different proportion of life-history traits, where macropterous species are gradually replaced by brachypterous species associated with a forest habitat. We assume that another important phenomenon of successional changes at post-industrial sites are irregular disturbances of vegetation cover. Habitats with bare ground are created due to anthropic activities, which need not depend on spoil heap age. The species structure of such habitats also seemed to be random and without similar functional traits. The substitution of open habitat species with forest species during about 30 years of succession shows a relatively rapid process of primary succession on spoil heaps. We propose further monitoring of spoil heaps to elucidate the trends of FD in mature successional seres.

Acknowledgements We would like to thank Jiri Stanovsky and Jiri Vavra for their kind help concerning epigeic beetle ecology. We are also grateful to Monika Mulkova and Tomas Adamec, who helped us calculate the areas of the spoil heaps using ArcGIS software. This study was funded by the LO1208 project from the National Feasibility Programme I, grant no. SGS33/PRF/2014 from the University of Ostrava and grant reg. no. CZ.1.05/2.1.00/03.0100 and the research development project no. RVO 67985939 from the Institute of Botany,

Please cite this article in press as: Hodecek, J., et al. Post-industrial areas as successional habitats: Long-term changes of functional diversity in beetle communities. Basic and Applied Ecology (2015), http://dx.doi.org/10.1016/j.baae.2015.06.004

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Academy of Sciences of the Czech Republic. The work was supported by the Research and Development for Innovations Operational Programme financed by the Structural Funds of the European Union, the state budget of Czech Republic, reg. no. CZ.1.07/2.2.00/28.0149.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.baae.2015.06.004.

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