Abstract
Semi-natural linear landscape elements such as road verges, hedgerows and field margins are important in maintaining the connectivity between habitat fragments of highly modified landscapes. Preservation of habitat specialist fauna requires conservation of the remaining natural habitat patches and connectivity of fragments. Our study focuses on the spider, ant and true bug fauna and functional diversity (FD) of fragmented forest steppe patches, moderately grazed pastures and road verges embedded in a matrix of forest plantations in Hungary, Central Europe. We established total 30 sampling sites, 10 in each, the grassland component of forest-steppes (F), pastures (P) and road verges (R) near pine forests. We collected arthropods with pitfall and sweep-net techniques. We calculated FD and species composition of arthropods using linear mixed models. We observed higher species richness in road verges for spiders and ants. We also found higher FD values for spiders and different trait composition for all taxa in road verges when compared with forest steppes and pastures. Species composition suggests that road verges do not serve as habitat for several forest-steppe and grassland species, in spite of the fact that numerous specialist species were found in the road verges. We show that forest steppes have higher species richness of spiders than pastures, and there are differences in species assemblage composition of the two habitat types for all taxa. Our results indicate that road verges should be considered as an important refuge for grassland specialist arthropods, as road verges provide secondary linear habitats for many arthropod species, and we would suggest the maintenance of these grassy strips in order to preserve arthropod biodiversity.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
In fragmented agricultural landscapes of Europe, the availability of natural, semi-natural habitats has been highlighted as the limiting factor for the conservation of populations. Preservation of habitat specialist fauna in fragmented habitats requires conservation of natural habitat patches and connectivity of fragments. Artificial linear landscape elements (LLEs) are landscape structures established for a special function such as transportation on roads and drainage by ditches, but they have a part covered by vegetation, which is not directly used for its original function, and may potentially constitute semi-natural habitats. It is shown that a significant proportion of native biota can survive in LLEs such as ditch banks (Torma et al. 2018) field margins and hedgerows (Ernoult et al. 2013; Gallé et al. 2018a; Haaland et al. 2011; Morandin and Kremen 2013), road and railway verges (Henneberg et al. 2017; Jakobsson et al. 2018; Noordijk et al. 2009). These LLEs are important in conserving various arthropods and other animals as they can decrease isolation effect of fragmented habitats (Dover et al. 2000; Hinsley and Bellamy 2000; MacDonald 2003; Hollmen et al. 2008) and also, they function as corridors and refuges for species within highly modified landscapes (Zanden et al. 2013). Road verges between patches, for example, proved to have importance in conserving grassland specialist fauna in Ireland (Fuller et al. 2013) and also Noordijk et al. (2009) showed that apart from indigenous species of ants, grasshoppers, spiders, ground beetles, bees and butterflies, road verges were able to save several threatened species of grasshoppers and bees in intensively used landscapes in the Netherlands. LLEs can help in increasing species movements across the fragment habitat (Gilbert-Nortan et al. 2010). Although, road verges in fragmented habitats usually undergo management activities like mowing and subsequently changing the composition of communities. Careful management and preservations of road-side verge can help to protect biota (Le Viol et al. 2008; Decleer et al. 2015).
Forest-steppes are defined as an alternation of forest patches within steppe grasslands forming a mosaic-like structure (Erdős et al. 2014). An extensive forest-steppe belt has been developed in the Eurasian temperate zone under semi-humid to semi-arid climate, and it runs from the Pannonian lowland to China. The westernmost occurrence of forest-steppe is in the Hungarian Great Plain, where open forest patches are embedded in xeric grasslands (Erdős et al. 2018). Since grasslands are characterized by a higher temperature and lower humidity than forests, both habitat types have their own specialised fauna (Gallé et al. 2018b). Hungarian forest-steppes have lost more than 93% of their original areas during the past 200 years. The most important threatening factors of this habitat type and its high of conservation value invertebrate fauna are afforestation, overgrazing and desertification due to the drop of groundwater table and climate change (Molnár et al. 2012).
The majority of forest steppes in Hungary are altered by anthropogenic activities such as forest management to meet the growing forestry demands and to stabilize the sandy soil in open grasslands (Molnár et al. 2012). In addition to native deciduous forest plantations, exotic species like black locust (Robinia pseudoacacia) and scots pine (Pinus sylvestris) were introduced to the Great Hungarian Plain at the beginning of the seventeenth and at the end of the nineteenth century, respectively (Redei et al. 2008; Masón and Alía 2000). In this region, there also exists extensive sandy grasslands, that are regularly used for pasture and maintained by sheep or cattle grazing thus they are in a semi-natural form (Biró et al. 2013). Intensive management of these grasslands threatens biodiversity (Dengler et al. 2012). However, grasslands with sparse woody vegetation and are moderately grazed can maintain diverse species richness (Kőrösi et al. 2011; Gallé et al. 2017). Overgrazing of the grasslands on the other hand leads to structural simplification of the habitat, and thus have negative effect on arthropod fauna (Horváth et al. 2009; Habel et al. 2013).
Arthropods represent a widely used indicator group in conservation studies, as they are highly diverse and present in almost every terrestrial and aquatic habitat. They interact with various other groups and are important mediators of ecosystem. In our study, we focused on three arthropod taxa, spiders (Araneae), true bugs (Heteroptera) and ants (Hymenoptera: Formicidae). Spiders are among the most abundant invertebrate predators, that play a decisive role in the regulation of other invertebrate assemblages (Clarke and Grant 1968; Moulder and Reichle 1972; Weeks and Holtzer 2000). The diversity of spiders is affected by a number of environmental factors that directly control their microhabitat requirements (Ziesche and Roth 2008). True bugs are the largest and most diverse group of hemimetabolous insects. They comprise phytophagous, zoophagous and omnivorous feeders (Fauvel 1999). Their presence in particular habitat reflects habitat condition primarily determined host plants for phytophagous and omnivorous species, whereas vegetation structure and prey availability specify the suitable habitat for zoophagous species (Gallé et al. 2010). Ants are one of the most ecologically important animal groups in many terrestrial ecosystems. They are highly diverse, abundant, sensitive to change in the environment and can provide cost effective and efficient data compared to other invertebrate groups (Andersen and Majer 2004). They play complex role as predators, herbivores, seed-dispersal agents and soil engineers (Hölldobler and Wilson 1990). Any change in their micro or macrohabitat such as shading effect, soil type or vegetation cover directly affect their community structure in nature (Andersen et al. 2002). Ants respond quickly to changes in their habitat such as the clearing of forests (Majer et al. 1997), road construction (Lassau and Hochuli 2004), anthropogenic disturbances or agricultural practices (Evans et al. 2011) hence, are reliable bioindicators.
Traditionally, species richness has been used as a diversity measure of ecosystems, neglecting the functional diversity (FD) approach. However, change in the FD of species corresponds to all the functions provided by these species in an ecosystem, thereby being able to predict ecosystem processes, dynamics and stability (Petchey and Gaston 2006). Therefore, FD provides a more accurate picture of the change of ecosystems due to changes in habitats (Díaz and Cabido 2001).
In this research, we aim to study the species richness and FD of the arthropod fauna of forest-steppe patches, pastures, and road verges within exotic forest plantations. We focus on addressing the following questions: (1) Do linear grassy strips along road verges have a role in maintaining the steppe species of arthropods? (2) Are the forest-steppe grasslands different from pastures in terms of arthropod species composition and FD (functional trait composition, RaoQ diversity)? (3) Is there any difference in the species composition between the studied habitat types?
Materials and methods
Study region
Our study was conducted in the southern part of Hungary, in the Danube–Tisza Interfluve (47.1625°N, 19.5033°E, elevation approximately 100 m asl, Fig. 1). The climate is continental with some Mediterranean influence (Borhidi 1993). Mean annual precipitation is 500–550 mm, which decreases from NW to SE, and the mean annual temperature is ca. 10 °C with a semi-arid period in late summer (Fekete et al. 2002). The soil is a sandy silt and loess rich soil, which were originally formed through regular flooding of the Danube River. The main natural habitat type of the study region is a forest-steppe. The typical vegetation of grassland component of forest-steppe consists of drought tolerant tall grasses, mainly Festuca vaginata and Stipa borysthenica coupled with few dicots such as Alkanna tinctoria, Dianthus serotinus, Fumana procumbens, Iris arenaria and Onosma arenaria (Molnár et al. 2012; Erdős et al. 2015). Road verges consist of generalist plant species along with some steppe grassland species such as F. vaginata, S. borysthenica and A. tinctoria (personal observation).
Study sites and sampling design
Ten sites in each habitat, the grassland component of forest-steppes (F), pastures (P) and road verges (R) near pine forests were assigned for sampling, respectively. We excluded potential sampling sites with significant cover of invasive plant species like Asclepias syriaca, R. pseudoacacia and Ailanthus altissima. All study sites were in the range of approximately 50 km and were minimum 1 km apart and around four villages (Zsana, n = 5; Imrehegy, n = 3; Pirtó, n = 7; Tázlár, n = 15) In each site, four pitfall traps were arranged in a transect at 5 m intervals to sample ground-dwelling arthropods. Traps were 500 ml white plastic cups, 8.5 cm in diameter, and they were provided with a metal roof and plastic funnel to prevent the preservative from dilution by rain or entry of vertebrates (Császár et al. 2018). We used 50/50 ethylene glycol/water mixture in pitfall traps as a preservative. In addition to pitfall traps, we also used sweep net technique to sample vegetation dwelling arthropods. At each site, we collected 5e samples, each comprised of 25 sweeps along ca. 20 m transect. Pitfall traps were open twice between 6th and 16th June and between 11th and 26th September 2017, respectively. Sweep net sampling was done on the 16th of June and the 26th of September. Data were pooled per site for further analysis. We identified the collected invertebrates using the keys of Nentwig et al. (2019) for spiders, and key of Czechowski et al. (2012) for ants. To identify true bugs, we used various keys (Wagner and Weber 1964; Schuh et al. 1995; Matocq 2004; Rabitsch and Deckert 2007). Voucher specimens were stored in the collection of the Department of Ecology, University of Szeged, Hungary.
Data analysis
We used three ecological traits to characterize the sampled arthropod species: moisture preference, shading tolerance and dispersal ability (Table 1). Species were assigned with a specific value from 0 to maximum 5 for each trait. If a given species felt under more than one category, then an averaged value was assigned. Generalist species or species with no data available in any trait category were excluded from further calculations. Species were considered as generalist if they fell under more than the half of the categories. All trait values were ranged between 0 and 1 to account for the different number of categories. We did not perform any statistical analysis on the dispersal ability of ants because the overwhelming majority of the collected species disperse only by nuptial flight.
We calculated the single trait FD measure, community weighted mean (CWM) for all traits of the three arthropod groups, and we used the multivariate RaoQ index to characterize FD of our sampling sites with the FD package in R (Laliberté et al. 2014).
We used linear mixed models to determine the effect of habitat type as fixed effect (i.e., F, P or R) and villages as a random effect on species richness and FD indices. We used negative binomial and Poisson error term for species richness after checking for overdispersion of data for spiders, true bugs and ants respectively. We used Gaussian error term for CWM and RaoQ indices. Pairwise comparisons were carried out using the “relevel” function in R.
We performed analysis of similarities (ANOSIM) based on Bray–Curtis dissimilarity matrices with 10,000 permutations to test the multivariate differences among the arthropod assemblages in the three habitats types using “anosim” function of the vegan package in R (Oksanen et al. 2015). We visualized this data set with non-metric multidimensional scaling based on the Hellinger transformation (Legendre and Gallagher 2001) using vegan package 2.4-6. A maximum number of 20 random starts were used to search for a stable solution to fit into the two-dimensional plot. We also performed an indicator value analysis to identify the characteristic species in forest steppe, pastures and road verges (IndVal; Dufrene and Legendre 1997) with the ‘labdsv’ package (Roberts 2012).
Results
We collected a total of 6983 spider individuals (out of which 1598 were adults and could be identified to species level and for all others that follow), 5537 adult true bugs and 16,425 adult ants from 114, 147 and 27 species, respectively. Altogether, we found 72 spider, 85 true bug and 19 ant species in forest steppe grasslands; 51 spider, 87 true bug and 16 ant species in pastures; and 75 spider, 92 true bug and 22 ant species in road verges. Among spiders, Oxyopes heterophthalmus (Latreille, 1804), Tibellus macellus (Simon, 1875) and Zelotes longipes (L. Koch, 1866) were the most common, comprising approximately 35% of all individuals. True bugs were largely represented by the rhopalids, and Rhopalus parumpunctatus (Schiling, 1829) and Chorosoma gracile (Josifov, 1968) were the most abundant species, together more than 27% of the total catch. The most abundant ant species were Plagiolepis taurica (Santschi, 1920), Lasius psammophilus (Seifert, 1992) and Tetramorium cf. caespitum (Linnaeus, 1758), accounting for approximately 70% of all individuals.
Linear stripes along the road verges had higher species richness of spiders and ants than pastures, however, true bug species richness was similar in all three habitats (Table 2). Road verges had higher spider FD (RaoQ) than the other two habitat types (Table 2). We also found higher moisture preference values in the road verges than in the other two habitat types for all arthropods, furthermore, CWM shading tolerance was also higher in the road verges for spiders and true bugs than in forest-steppes and pastures (Table 2). The highest dispersal CWM values were also found in road verges for true bugs, however, we did not find any significant difference in the dispersal ability of spiders.
We found significant differences in the species composition of spiders (ANOSIM: R = 0.282, p < 0.001), true bugs (ANOSIM: R = 0.4774, p < 0.001), and ants (ANOSIM: R = 0.211, p < 0.001) between habitats. Road verges and pastures were the most distinct habitat pair, with little overlap between them according to the NMDS scatterplot (Fig. 2). Significant indicator species in all three habitats were found for true bugs (19), followed by spiders (15) and ants (6) (see Appendix 4). Majority of the indicator value species of true bugs in road verges were dry grassland species (e.g., D. spinolae, N. tipularis and Catoplatus carthusianus), wet meadow (e.g. L. simulans) along with some habitat generalist species (e.g. Palomena prasina). Spiders were represented by xerothermic (e.g. Z. electus, Z. apricorum and P. minimus), habitat generalist (e.g. T. terricola, Pardosa alacris and Zodarion germanicum), grassland species (e.g. M. acalypha) and forest species (e.g. P. tincta). Ants population in road verges were generalist (e.g. T. unifasciatus), xerothermic grassland (e.g. Temnothorax interruptus) and dry forest species (e.g. Formica sanguinea).
Discussion
In this research we aimed to assess the importance of road verges in maintaining the arthropod fauna of forest-steppes. We compared species composition and FD of forest steppe grasslands and pastures with road verges. We observed higher species richness in road verges than in pastures for spiders and ants. We also found high FD values for spiders and different trait composition for all taxa in road verges when compared with forest-steppes and pastures. The characteristic species composition and the high number of indicator species for pastures and forest-steppes suggest that road verges do not serve as habitat for several grassland and forest-steppe species, in spite of the fact that numerous specialist species were found in the road verges, as well. We found that the grassland component of forest-steppes has higher species richness of spiders than pastures, and we found differences in species composition of the two habitat types for all taxa based on the multivariate analyses.
The role of road verges in maintaining arthropod biodiversity within intensively managed landscape is increasingly recognised (Schaffers et al. 2012; Reck and van der Ree 2015), as they may serve as linear habitats and dispersal corridors for weak-flying insects (Vermeulen 1994) and overwintering habitat for several specialists (Schaffers et al. 2012; Gallé et al. 2018a). In native forests, however, road verges may have a negative impact on the biota, fragmenting forest habitats by exerting barrier effects on the forest specialist species (Yamada et al. 2010). Furthermore, they may also support invasive species (Smith et al. 2007). In our study, road verges were inhabitated partly by forest species from pine plantations [e.g., spiders: P. alacris (C. L. Koch, 1833) and Z. germanicum (C. L. Koch, 1837), ants: F. sanguinea (Latreille, 1798)]. The higher CWM shading values in road verges as compared to pastures also indicated the relatively high number of forest species. Besides forest species, we also collected open habitat generalists [e.g., spiders: O. heterophthalmus (Latreille, 1804), true bugs: P. prasina (Linnaeus, 1761), ants: T. interruptus (Schenck, 1852)] and several steppe species [e.g., spiders: Gnaphosa mongolica (Simon, 1895), true bugs: C. carthusianus (Goeze, 1778)]. Thus, road verges between exotic plantations may act as secondary habitats for several specialist arthropod species. In line with these results, Koivula (2003) found that the narrow forest roadside verges are preferred by open-habitat and generalist carabid beetles.
Pine plantation forests have a relatively simple habitat structure due to the closed canopy (Gallé et al. 2014). Compared to the interior of exotic plantations, road verges between exotic forests have more open spaces, which can regulate microhabitat conditions, species composition of vascular plants and structure of the vegetation (Mullen et al. 2003; Smith et al. 2007). The dense vegetation along road verges provides high diversity of potential food for true bugs and ants, and it substantially increases the number of potential web attachment points for web-building spiders and may increase the species richness.
Moisture preference CWM values were consistently highest in road verges for all the studied taxa. This may correspond with a temperature gradient. Sandy dry pastures of the Kiskunság region often exhibit very high surface temperature during summer that can reach 60 °C (Erdős et al. 2014), and as a consequence of evaporation, there is a very low soil water content near the soil surface. These climatic parameters act as strong environmental filters (Entling et al. 2007), and as a consequence, sandy pastures have a specialized, thermophilous and xerotolerant fauna. This environmental filter reduces the diversity of trait values, resulting in low RaoQ values (Gallé et al. 2018b). Certainly, this does not imply the higher conservation value of road verges compared to grasslands and pastures.
Road verges were associated with the highest dispersal trait values for true bugs according to the linear mixed models. These narrow grassy strips in pine plantations are low quality secondary habitats for the forest-steppe fauna of true bugs, and the regular disturbance may preclude the effective colonization of several wingless species. Dispersal ability clearly influences the colonization of true bugs (Moir et al. 2005), resulting in higher dispersal trait values of true bugs in more disturbed habitats (Torma et al. 2019). Well-dispersing species with developed wings can travel long distances (presumably several kilometres, see Kiritani and Sasaba 1969), but they probably travel as far as necessary to locate the nearest host plant or suitable habitat patch (Tillman et al. 2009). The type of vegetation and land use primarily affects the species composition and richness of true bug assemblages (Zurbrügg and Frank 2006; Torma and Császár 2013; Torma et al. 2017), thus, besides dispersal limitation, specialized habitat requirements of species and the density of potential host plants may be the most important determinants of colonization pattern of true bugs in road verges.
Conclusion
Our study emphasizes the importance of road verges in exotic plantations for the conservation of arthropod diversity. With the change of natural habitats to exotic or semi-natural forests, it is important to maintain every aspect of this grassland habitat that has the capability to protect this unique biodiversity. Our results indicate that road verges should be considered an important reserve for grassland specialists, as they provide secondary linear habitats for many arthropod species. Road verges are often maintained by forestry management, and this disturbance may reduce their conservation capabilities. We suggest the maintenance of these grassy strips in order to preserve arthropod biodiversity.
References
Andersen AN, Majer JD (2004) Ants show the way Down Under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298
Andersen AN, Hoffmann BD, Muller WJ, Griffiths AD (2002) Using ants as bioindicators in land management: simplifying assessment of ant-community responses. J Appl Ecol 39:8–17
Bell JR, Bohan DA, Shaw EM, Weyman GS (2005) Ballooning dispersal using silk: world fauna, phylogenies, genetics and models. Bull Entomol Res 95:69–114
Biró M, Szitár K, Horváth F, Bagi I, Molnár Zs (2013) Detection of long-term landscape changes and trajectories in a Pannonian sand region: comparing land-cover and habitat-based approaches at two spatial scales. Community Ecol 14:219–230
Blandenier G (2009) Ballooning of spiders (Araneae) in Switzerland: general results from an eleven-year survey. Arachnology 14:308–316
Borhidi A (1993) Characteristics of the climate of the Danube–Tisza Mid-region. In: Szujkó-Lacza J, Kováts D (eds) The flora of the Kiskunság National Park. Magyar Természettudományi Múzeum, Budapest, pp 9–20
Buchar J, Ruzicka V (2002) Catalogue of spiders of the Czech Republic. Peres, Prague
Clarke RD, Grant PR (1968) An experimental study of the role of spiders as predators in a forest litter community. Part 1. Ecology 49:1152–1154
Császár P, Torma A, Gallé-Szpisjak N, Tölgyesi C, Gallé R (2018) Efficiency of pitfall traps with funnels and/or roofs in capturing ground-dwelling arthropods. Eur J Entomol 115:15–24
Czechowski W, Radchenko A, Czechowska W, Vepsäläinen K (2012) The ants (Hymenoptera, Formicidae) of Poland with reference to the myrmecofauna of Europe. MIZ PAS, Warszawa
Decleer K, Maes D, van Calster H, Jansen I, Pollet M, Dekoninck W, Baert L, Grootaert P, van Diggelen R, Bonte D (2015) Importance of core and linear marsh elements for wetland arthropod diversity in an agricultural landscape. Insect Conserv Divers 8:289–301
Dengler J, Becker T, Ruprecht E, Szabó A, Becker U et al (2012) Festuco-Brometea communities of the Transylvanian Plateau (Romania): a preliminary overview on syntaxonomy, ecology, and biodiversity. Tuexenia 32:319–359
Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Dover J, Sparks T, Clarke S, Gobbet K, Glossop S (2000) Linear features and butterflies: the importance of green lanes. Agric Ecosyst Environ 80:227–242
Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–367
Entling W, Schmidt MH, Bacher S, Brandl R, Nentwig W (2007) Niche properties of Central European spiders: shading, moisture and the evolution of the habitat niche. Glob Ecol Biogeogr 16:440–448
Erdős L, Tölgyesi C, Horzse M et al (2014) Habitat complexity of the Pannonian forest-steppe zone and its nature conservation implications. Ecol Complex 17:107–118
Erdős L, Cs Tölgyesi, Cseh V et al (2015) Vegetation history, recent dynamics and future prospects of a Hungarian sandy forest-steppe reserve: forest-grassland relations, tree species composition and size-class distribution. Community Ecol 6:95–105
Erdős L, Ambarlı D, Anenkhonov OA et al (2018) The edge of two worlds: a new review and synthesis on Eurasian forest-steppes. Appl Veg Sci 21:345–362
Ernoult A, Vialatte A, Butet A, Michel N, Rantier Y, Jambon O, Burel F (2013) Grassy strips in their landscape context, their role as new habitat for biodiversity. Agric Ecosyst Environ 166:15–27
Evans TA, Dawes TZ, Ward PR, Lo N (2011) Ants and termites increase crop yield in a dry climate. Nat Commun 2:262
Fauvel G (1999) Diversity of Heteroptera in agroecosystems: role of sustainability and bioindication. In: Paoletti MG (ed) Invertebrate biodiversity as bioindicators of sustainable landscapes. Elsevier, Amsterdam, pp 275–303
Fekete G, Molnár Zs, Kun A, Botta-Dukát Z (2002) On the structure of the Pannonian forest steppe: grasslands on sand. Acta Zool Acad Sci Hung 48:137–150
Fuller L, Irwin S, Kelly T, O’Halloran J, Oxbrough A (2013) The importance of young plantation forest habitat and forest road-verges for ground-dwelling spider diversity. Biol Environ 113:259–271
Gallé R, Torma A, Körmöczi L (2010) Small-scale effect of habitat heterogeneity on invertebrate assemblages in sandy grasslands (Hungarian Great Plain). Pol J Ecol 58:333–346
Gallé R, Kanizsai O, Ács V, Molnár B (2014) Functioning of ecotones—spiders and ants of edges between native and non-native forest plantations. Pol J Ecol 62:815–820
Gallé R, Urak I, Nikolett G-S, Hartel T (2017) Sparse trees and shrubs confers a high biodiversity to pastures: case study on spiders from Transylvania. PLoS ONE 12(9):e0183465
Gallé R, Császár P, Makra T et al (2018a) Small-scale agricultural landscapes promote spider and ground beetle densities by offering suitable overwintering sites. Landsc Ecol 33:1435–1446
Gallé R, Szabó Á, Császár P, Torma A (2018b) Spider assemblage structure and functional diversity patterns of natural forest steppes and exotic forest plantations. For Ecol Manag 411:234–239
Gilbert-Nortan L, Wilson R, Stevens JR, Beard KH (2010) A meta-analytic review of corridor effectiveness. Conserv Biol 24:660–668
Haaland C, Naisbit RE, Bersier LF (2011) Sown wildflower strips for insect conservation: a review. Insect Conserv Divers 4:60–80
Habel JC, Dengler J, Janisova M, Torok P, Wellstein C, Wiezik M (2013) European grassland ecosystems: threatened hotspot of biodiversity. Biodivers Conserv 22:2131–2138
Henneberg P, Bogusch P, Rĕzáč M (2017) Roadside verges can support spontaneous establishment of steppe-like habitats hosting diverse assemblages of bees and wasps (Hymenoptera: Aculeata) in an intensively cultivated Central European landscape. Biodivers Conserv 26:843–864
Hinsley SA, Bellamy PE (2000) The influence of hedge structure, management and landscape context on the value of hedgerows to birds: a review. J Environ Manag 60:33–49
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University, Cambridge, p 732
Hollmen A, Valimaki P, Itamies J, Oksanen J (2008) The value of open power line habitat in conservation of ground beetles (Coleoptera: Carabidae) associated with mires. J Insect Conserv 12:163–177
Horváth R, Magura T, Szinetár C, Tóthmérész B (2009) Spiders are not less diverse in small and isolated grasslands, but less diverse in overgrazed grasslands: a field study (east Hungary, Nyírség). Agric Ecosyst Environ 130:16–22
Jakobsson S, Bernes C, Bullock JM, Verheyen K, Lindborg R (2018) How does roadside vegetation management affect the diversity of vascular plants and invertebrates? A systematic review. Environ Evid 7:17
Kiritani K, Sasaba T (1969) The difference in bio- and ecological characteristics between neighbouring populations in the southern green stink bug, Nezara viridula L. Jpn J Ecol 19:177–184
Koivula M (2003) The forest road network—a landscape element affecting the distribution of boreal carabid beetles (Coleoptera, Carabidae). In: Szyszko J, den Bor PJ, Bauer T (eds) How to protect or what we know about carabid beetles. University of Warsaw Press, Warsaw, pp 287–300
Kőrösi A, Batary P, Orosz A, Redei D, Baldi A (2011) Effects of grazing, vegetation structure and landscape complexity on grassland leafhoppers (Hemiptera: Auchenorrhyncha) and true bugs (Hemiptera: Heteroptera) in Hungary. Insect Conserv Divers 5:57–66
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12
Lassau SA, Hochuli DF (2004) Effects of habitat complexity on ant assemblages. Ecography 27:157–164
Le Viol I, Julliard R, Kerbiriou C, Redon L et al (2008) Plant and spider communities benefit differently from the presence of planted hedgerows in highway verges. Biol Conserv 14:1581–1590
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
MacDonald MA (2003) The role of corridors in biodiversity conservation in production forest landscapes: a literature review. Tasforests 14:41–52
Majer JD, Delabie JHC, McKenzie NL (1997) Ant litter fauna of forest, forest edges and adjacent grassland in the Atlantic rain forest region of Bahia, Brazil. Insectes Soc 44:255–266
Masón WL, Alía R (2000) Current and future status Scots pine (Pinus sylvestris L.) forests in Europe. For Syst 9:317–335
Matocq A (2004) Review of the species assigned to the genus Megalocoleus Reuter, 1890 (Heteroptera: Miridae). Ann Soc entomol Fr (NS) 40:69–101
Moir ML, Brennan KEC, Koch JM, Majer JD, Fletcher MJ (2005) Restoration of a forest ecosystem: the effects of vegetation and dispersal capabilities on the reassembly of plant-dwelling arthropods. For Ecol Manag 217:294–306
Molnár Zs, Biró M, Bartha S, Fekete G (2012) Past trends, present state and future prospects of Hungarian forest-steppes. In: Werger M, van Staalduinen M (eds) Eurasian steppes. Ecological problems and livelihoods in a changing world. Springer, Dordrecht, pp 209–252
Morandin LA, Kremen C (2013) Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecol Appl 23:829–839
Moulder BC, Reichle DE (1972) Significance of spider predation in the energy dynamics of forest-floor arthropod communities. Ecol Monogr 4:473–498
Mullen K, Fahy O, Gormally M (2003) Ground flora and associated arthropod communities of forest road edges in Connemara, Ireland. Biodivers Conserv 12:87–101
Nentwig W, Blick T, Gloor D, Hänggi A, Kropf C (2019) Spiders of Europe. https://www.araneae.nmbe.ch. Accessed 20 Feb 2019
Noordijk J, Raemakers IP, Schaffers AP, Sykora KV (2009) Arthropod richness in roadside verges in Netherlands. Terr Arthropod Rev 2:63–76
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al (2015) Vegan: community ecology package. R package version 2.3-0. http://CRAN.R-project.org/package=vegan. Accessed 08 Oct 2018
Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758
Rabitsch W, Deckert J (2007) Die Ritterwanze Lygaeus equestris LINNAEUS, 1758 (Heteroptera: Lygaeidae) – das Insekt des Jahres 2007. Beitr Entomofaunist 8:212–218
Reck H, van der Ree R (2015) Insects, snails and spiders: the role of invertebrates in road ecology. In: van der Ree R, Smith DJ, Grilo C (eds) Handbook of road ecology. Wiley, Chichester, pp 247–257
Redei K, Osvath-Bujtas Z, Veperdi I (2008) Black locust (Robinia pseudoacacia L.) improvement in Hungary: a review. Acta Silv Lignaria Hung 4:127–132
Roberts DW (2012) Package “labdsv”. http://cran.r-project.org/web/packages/labdsv/labdsv.pdf. Accessed 10 Oct 2018
Schaffers AP, Raemakers IP, Sýkora KV (2012) Successful overwintering of arthropods in roadside verges. J Insect Conserv 16:511–522
Schuh RT, Lindskog P, Kerzhner IM (1995) Europiella Reuter (Heteroptera: Miridae): recognition as a Holarctic group, notes on synonymy, and description of a new species, Europiella carvalhoi, from North America. Proc Entomol Soc Wash 97:379–395
Smith GF, Iremonger S, Kelly DL, O’Donoghue S, Mitchell FJG (2007) Enhancing vegetation diversity in glades, rides and roads in plantation forests. Biol Conserv 136:283–294
Tillman PG, Northfield TD, Mizell RF, Riddle TC (2009) Spatiotemporal patterns and dispersal of stink bugs (Heteroptera: Pentatomidae) in peanut-cotton farmscapes. Environ Entomol 38:1038–1052
Torma A, Császár P (2013) Species richness and composition patterns across trophic levels of true bugs (Heteroptera) in the agricultural landscape of the lower reach of the Tisza River Basin. J Insect Conserv 17:35–51
Torma A, Bozsó M, Tölgyesi C, Gallé R (2017) Relationship of different feeding groups of true bugs (Hemiptera: Heteroptera) with habitat and landscape features in Pannonic salt grasslands. J Insect Conserv 21:645–656
Torma A, Bozsó M, Gallé R (2018) Secondary habitats are important in biodiversity conservation: a case study on orthopterans along ditch banks. Anim Biodivers Conserv 41:97–108
Torma A, Császár P, Bozsó M, Deák B, Valkó O, Kiss O, Gallé R (2019) Species and functional diversity of arthropod assemblages (Araneae, Carabidae, Heteroptera and Orthoptera) in grazed and mown salt grasslands. Agric Ecosyst Environ 273:70–79
Vermeulen HJ (1994) Corridor function of a road verge for dispersal of stenotopic heathland ground beetles Carabidae. Biol Conserv 69:339–349
Wachmann E, Melber A, Deckert J (2004–2012) Wanzen. Band 1–5 Die Tierwelt Deutschlands. Goecke and Evers, Keltern
Wagner E, Weber HH (1964) Hétéroptères. Miridae. Fauna de France 67. Fédération Française des Sociétés de Sciences Naturelles, Paris, p 590
Weeks RD Jr, Holtzer TO (2000) Habitat and season in structuring ground-dwelling spider (Araneae) communities in a shortgrass steppe ecosystem. Environ Entomol 29:1164–1172
Yamada Y, Sasaki H, Harauchi Y (2010) Effects of narrow roads on the movement of carabid beetles (Coleoptera, Carabidae) in Nopporo Forest Park, Hokkaido. J Insect Conserv 14:151–157
Zanden EH, Verburg PH, Mücher CA (2013) Modelling the spatial distribution of linear landscape elements in Europe. Ecol Indic 27:125–136
Ziesche TM, Roth M (2008) Influence of environmental parameters on small-scale distribution of soil-dwelling spiders in forests: what makes the difference, tree species or microhabitat? For Ecol Manag 255:738–752
Zurbrügg C, Frank T (2006) Factors influencing bug diversity (Insecta: Heteroptera) in semi-natural habitats. Biodivers Conserv 15:275–294
Acknowledgements
Open access funding provided by University of Szeged (SZTE). This work was supported by the Hungarian National Research, Development and Innovation Office (Grant ID NKFH-FK-124579). HK is supported by Stipendium Hungaricum Scholarship of Tempus Public Foundation. RG was supported by Bolyai Scholarship of the MTA.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The study did not involve endangered or protected species and we did not collect arthropods in protected areas.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Kaur, H., Torma, A., Gallé-Szpisjak, N. et al. Road verges are important secondary habitats for grassland arthropods. J Insect Conserv 23, 899–907 (2019). https://doi.org/10.1007/s10841-019-00171-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-019-00171-9