Calcareous grasslands are among the most species-rich habitats in Europe, but are increasingly threatened due to abandonment and fragmentation. Little is known about how the surrounding landscape influences fragmentation effects. Here, we focus on the interaction between habitat fragmentation and landscape composition on leafhoppers, a highly diverse group of insects, including many species that are likely to be vulnerable to changes in their environment.
We selected 14 small and 14 large fragments of calcareous grassland in Central Germany, differing in isolation from other calcareous grasslands and in composition of the surrounding landscape. Leafhoppers, sampled by sweep netting, were either specialists that depended on calcareous grasslands or generalists that could use the landscape matrix, but still required low-productivity habitats.
Increasing habitat isolation reduced leafhopper species richness in simple (dominated by arable crops), but not in complex landscapes. This effect was driven by the generalist species. In simple landscapes, leafhoppers may find it more difficult to reach the next suitable fragment due to a lack of alternative resources during dispersal.
Moreover, we found that generalist species richness increased with increasing connectivity on small fragments, whereas it remained stable with increasing connectivity on large fragments. In small, isolated fragments, a higher extinction rate combined with a lower probability of recolonization is thought to cause the reduced species richness.
Synthesis and applications. Our results show for the first time that insect species richness can be negatively affected by increasing habitat isolation in simplified but not in complex landscapes and in small but not in large fragments. We provide evidence that mitigating the negative effects of habitat fragmentation needs to take the surrounding landscape into account. Management efforts should prioritize (i) an increase in connectivity of small, isolated fragments, (ii) an increase in connectivity of fragments in simple landscapes and (iii) enhanced dispersal by increasing heterogeneity of both landscape composition and configuration. Moreover, extensive management of fragments by grazing or mowing to increase local habitat quality for leafhoppers would benefit other insect groups as well.
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Habitat fragmentation, habitat loss and landscape modification are the main drivers of biodiversity loss (Sala et al. 2000; Fahrig 2003; Foley et al. 2005; Fischer & Lindenmayer 2007). In Central Europe, semi-natural calcareous grasslands harbour an exceptional diversity of organisms, including plants (Ellenberg & Leuschner 2010), insects (Krauss, Steffan-Dewenter & Tscharntke 2003; van Swaay 2002) and snails (Boschi & Baur 2007). Unfortunately, since the onset of agricultural intensification and the abandonment of historic land use practices like extensive grazing (Poschlod & WallisDeVries 2002), a large part of this highly diverse habitat type has been lost (for Germany: Riecken, Ries & Ssymank 1994). For example, in the Swabian Alb in Southern Germany, more than 70% of the calcareous grasslands that were present in the year 1900 have disappeared (Mattern, Mauk & Kübler 1992). Therefore, connectivity of the remaining sites has been reduced dramatically. For example, floral connectivity has decreased due to the abandonment of transhumance shepherding, which ensured the dispersal of plant propagules (Poschlod & WallisDeVries 2002). Long-lived organisms like plants are able to persist for a longer period of time in fragmented, isolated habitats than short-lived organisms like most invertebrates (‘extinction debt’, Tilman et al. 1994; Piqueray et al. 2011). All these changes in management pose a severe threat for the specialized plant and invertebrate species confined to calcareous grasslands (Fischer & Stöcklin 1997; Niemelä & Baur 1998).
According to the theory of island biogeography (Losos & Ricklefs 2010), the species diversity of islands is determined by both extinction and immigration. Island habitats that are more isolated – in this case, fragments of calcareous grassland in a ‘sea’ of intensively managed agricultural matrix – are less likely to receive immigrants from other islands. Smaller islands have a lower probability of receiving immigrants than larger ones and face higher extinction rates due to stochastic events (Whittaker 1992), while larger islands harbour more species due to larger variety of (micro)habitats and enhanced apparency for dispersers. It nevertheless needs to be kept in mind that considering habitat fragments as surrounded by an entirely hostile matrix may be an oversimplification (Debinski 2006; Ewers & Didham 2006; Prugh et al. 2008). Eycott et al. (2012) and Öckinger et al. (2012) showed that different matrix types can either facilitate or hinder migration of organisms.
Within the study area (District Göttingen, Lower Saxony, Germany), there are still supposed to be more than 200 fragments of calcareous grassland. However, they only cover about 0·3% of the area and frequently are of low quality due to a lack of management (pers. obs.). In the area, there have been studies on butterflies, hoverflies and bees of calcareous grasslands (Krauss, Steffan-Dewenter & Tscharntke 2002; Meyer, Gaebele & Steffan-Dewenter 2007), showing a positive relationship between habitat area and insect diversity as well as a positive effect of landscape diversity on both species richness and abundance.
In this study, we focus on the effects of three landscape parameters: habitat area (large vs. small fragments), connectivity (measured by a connectivity index described by Hanski, Alho & Moilanen (2000)) and landscape composition (represented by the amount of arable land within a 500-m buffer around each site). Additionally, we use plant species richness as a surrogate for habitat quality and resource availability.
As study organisms we chose leafhoppers, planthoppers and froghoppers (Auchenorrhyncha, hereafter referred to as leafhoppers), a very diverse group of plant sucking insects highly influenced by vegetation structure and composition (Novotný 1995; Nickel 2003). They include many specialist species that can be hypothesized to sensitively react to changing landscapes and fragmentation (Biedermann et al. 2005; Littlewood, Pakeman & Pozsgai 2012).
This study is the first to test how habitat area, connectivity and landscape composition interactively affect insect species richness (with a focus on leafhopper communities). We hypothesized that (i) there are fewer leafhopper species on isolated fragments than on connected ones, (ii) increasing amount of arable land surrounding the fragments negatively influences leafhopper species richness, and (iii) leafhopper species richness is higher on larger fragments (Tscharntke et al. 2012). (iv) Specialist species are hypothesized to be more severely affected by decreasing connectivity and landscape compositional heterogeneity (i.e. increasing proportion of arable land) than generalists. This study has wider implications for other taxa with relatively low mobility because they can be expected to be affected by the landscape variables in a similar way.
Materials and methods
The study area was located in the vicinity of the city of Göttingen in southern Lower Saxony in Central Germany (51∙5°N, 9∙9°E, see Appendix S1 in Supporting Information). The landscape is characterized by intensively managed agricultural areas with a dominance of cereal and rape fields and fertile meadows, interspersed with forests on hilltops and patchily distributed fragments of semi-natural habitats like calcareous grasslands, belonging to the plant association Mesobrometum erecti Koch 1926 (Ellenberg & Leuschner 2010). These grasslands are frequently located on steep slopes and are managed by mowing or grazing with sheep, goats, cattle or horses. Many smaller fragments have been abandoned, leaving them to succession (pers. obs.).
By analysing digital maps (ATKIS-DLM 25/1 Landesvermessung und Geobasisinformationen Niedersachsen 1991–1996, Hannover, Germany) with the geographical information system ArcGIS 10·0 (ESRI Geoinformatik GmbH, Hannover, Germany) and subsequent extensive field surveys in the study area, we selected 14 small (0∙1–0∙6 ha) and 14 large (1∙2–8∙8 ha) fragments of calcareous grassland (for an overview of the study area, see Appendix S1) along two orthogonal gradients: a landscape composition gradient, that is, an increasing percentage of arable land within a radius of 500 m around the fragments (27–77%, mean = 47%), and a habitat connectivity gradient, measured by a connectivity index described by Hanski, Alho & Moilanen (2000):
Aj is the area of the neighbouring fragment j (in m2), and dij is the edge-to-edge distance (in m) from the focal fragment i to the neighbouring fragment j. α is a species-specific parameter describing a species' dispersal ability, and β is a parameter that describes the scaling of immigration. Because we applied the connectivity index to an entire community, both scaling parameters α and β were set to 0∙5. The values of the connectivity index varied between 20 and 849 (mean = 244), with large values indicating high levels of connectivity. All calcareous grassland fragments within a radius of 2000 m around each study site were taken into account, to assure that for every fragment the connectivity index was greater than zero. In addition, we measured the edge-to-edge distance to the nearest neighbouring fragment for each study fragment, which ranged from 30 to 1900 m. To be classified as separate, there had to be a distance of at least 30 m from the focal fragment to the nearest one. If the nearest fragment was smaller than 0∙1 ha, the next nearest fragment larger than that was used. Both connectivity measures were strongly correlated (Spearman correlation, rho = 0∙78, S = 6501∙6, P <0∙001).
It was difficult to select fragments of similar quality, because management differed from fragment to fragment. Some were grazed, whereas on others, management had been abandoned. If fragments were mown, this could happen at different times throughout the season, although never before the first sampling, that is, the beginning of June. Fragments that were managed for the conservation of rare plants (orchids in particular) were not cut before August to ensure that the seeds could fully ripen. To assure that the fragments exhibited the characteristics of calcareous grasslands, we only included fragments that harboured more than ten of the plant species that are typical for calcareous grasslands in the study area (Krauss et al. 2004). We did not try to avoid differences in habitat quality and management, because we intended to mirror the actual condition of calcareous grasslands in the study area.
Leafhoppers were sampled by sweep netting (Heavy Duty Sweep Net, 7215HS, BioQuip, diameter: 38 cm) on six randomly distributed transects with homogeneous vegetation per fragment (20 sweeps each, i.e. 120 sweeps in total) in dry weather on three occasions in 2010 (at the beginning of June, at the end of July and at the beginning of September). Transects were approximately 10 m long and were at least 3 m away from each other within a fragment.
The specimens caught were transferred into alcohol (70% vol.) and identified to species level in the laboratory using Biedermann & Niedringhaus (2004) and Kunz, Nickel & Niedringhaus (2011). Specimens of species with woody host plants were excluded, except when saplings of a potential host tree were present on the transects. Otherwise, it was assumed that they had been dislodged from their host tree by wind. If the species' larvae used herbs or grasses as host plants and only the imagines fed on trees, specimens were included in the analysis.
The identification to species level of female specimens of several genera is not possible (e.g. Ribautodelphax, Anaceratagallia, Psammotettix) (Biedermann & Niedringhaus 2004; Kunz, Nickel & Niedringhaus 2011). Thus, if male specimens were present, female specimens were assumed to belong to the same species. If not, they were only identified to genus level. If males of more than one species of a genus were present, the number of females was assumed to mirror that of males.
All leafhopper species were classified into habitat specialists and generalists according to (i) their specific habitat requirements typical for calcareous grassland (i.e. warm and dry habitat conditions, short, grazed swards, open soil) and (ii) diet preferences (i.e. utilizing plants that exclusively occur on calcareous grasslands) based on Nickel & Remane (2002) and Nickel (2003). A species was classified as a habitat specialist when condition(s) (i) and/or (ii) was fulfilled; it was classified as a generalist when neither (i) nor (ii) was fulfilled.
In addition, they were subdivided according to their ability to fly, that is, the length of their wings, with Biedermann & Niedringhaus (2004). If a species was wing-dimorphic, that is, it could be both long and short winged, the predominant wing type was used for categorization.
At the beginning of June, the vegetation (only vascular plants) of each transect was recorded in botanical plots (one 1 × 5 m plot per transect) according to Wilmanns (1993). Plant species identification and nomenclature follow Seybold (2009). The plant species were subdivided into habitat specialists and generalists according to Krauss et al. (2004).
Both leafhopper and plant species richness of the six transects per fragment were summed up. The leafhoppers were also summed over the three sampling occasions. Statistical analyses were conducted with R, version R 2·15·1 (R Development Core Team 2012).
For analysis of overall leafhopper species richness and species richness of specialist and generalist leafhoppers, we used generalized linear models using Poisson errors with the following explanatory variables: (i) the percentage of arable land in a 500-m buffer around each fragment, (ii) fragment size (in ha, taken as a factor, either ‘large’ or ‘small’), (iii) habitat connectivity, measured by a connectivity index described by Hanski, Alho & Moilanen (2000) (log10-transformed to achieve a better fit of the models) and (iv) plant species richness per site. The explanatory variables were essentially uncorrelated (Table S1).
In the full models, two-way interactions between all the explanatory variables were included. For all three models, we performed an automated stepwise model selection by AIC (function ‘stepAIC’ in the package ‘MASS’ (Venables & Ripley 2002)). In all analyses, there was no indication of overdispersion.
Table 1. Mean ± SEM leafhopper and plant species richness (Sp R) on small (n = 14) vs. large (n = 14) sites
22·9 ± 1·2
22·4 ± 1·6
8·6 ± 0·8
9·5 ± 0·9
14·2 ± 1·2
12·9 ± 1·0
246·7 ± 22·5
258·5 ± 29·3
138·6 ± 18·1
160·8 ± 23·5
108·1 ± 19·4
97·7 ± 20·7
47·6 ± 3·3
55·1 ± 1·7
23·8 ± 2·1
28·8 ± 1·1
23·8 ± 2·0
26·3 ± 2·0
In the 28 fragments of calcareous grassland, we found 77 leafhopper species (Table S2), from 65 genera with 7073 adult specimens (with 3454 specimens caught on the small sites and 3619 specimens caught on the large sites), representing 13% of the German leafhopper fauna (Biedermann & Niedringhaus 2004; Kunz, Nickel & Niedringhaus 2011). Species richness ranged from 14 to 31 species per fragment (Table 1, Table S2, S3). Separation into habitat specialists and generalists resulted in 29 specialist and 48 generalist species. The four most abundant specialist leafhopper species were Turrutus socialis (18∙3% of total abundance), Doratura stylata (8∙5%), Adarrus multinotatus (7∙5%) and Neophilaenus albipennis (3∙5%). The four most abundant generalist species were Arocephalus longiceps (5∙7%), Philaenus spumarius (5∙1%), Mocydia crocea (4∙1%) and Verdanus abdominalis (3∙2%) (Table S2). In the botanical surveys, we recorded 168 plant species from 123 genera, comprising 65 specialist and 103 generalist species (including 22 tree and shrub species as saplings), with a minimum of 25 and a maximum of 65 species per site (Table 1, Table S3).
In the analysis of overall leafhopper species richness, we found an interaction between habitat connectivity and landscape composition. An increase in habitat isolation caused a reduction in leafhopper species richness in simple (high percentage of arable land), but not in complex landscapes (low percentage of arable land) (Table 2, Fig. 1a).
Table 2. Generalized linear models on the effects of landscape context (% arable land), fragment type (large or small), connectivity (log10(CI+1), a connectivity index described by Hanski, Alho & Moilanen 2000, log10-transformed) and plant species richness on (1) overall leafhopper species richness, (2) generalist leafhopper species richness and (3) specialist leafhopper species richness. Only variables included in the final models are shown
P-values <0∙05 are depicted in bold characters.
% arable land (Ar)
Fragment type (Type)
Ar × Conn
Type × Conn
Conn × plant SpR
Subsequent analysis of generalist and specialist leafhopper species richness separately revealed that this interaction was driven by the generalist leafhoppers (Table 2, Fig. 1b). The latter showed the same pattern as the overall species richness. The generalist leafhoppers showed an additional interaction: species richness on small fragments increased with increasing habitat connectivity, whereas it remained stable on large fragments (Table 2, Fig. 1c). There was an increase in generalist species richness with increasing plant species richness on both isolated and connected fragments. This increase, however, was steeper on connected fragments (Fig. 1d). Specialist leafhopper species richness was not affected by connectivity, landscape context or fragment size.
Generalist species richness per site was highly correlated with the number of long-winged (macropterous) species (Pearson correlation, r = 0∙83, t = 7∙58, d.f. = 26, P <0∙001), while the same was true for specialist species richness per site and short-winged (brachypterous) species (Pearson correlation, r = 0∙61, t = 3∙93, d.f. = 26, P <0∙001).
In this study, we found that generalist but not specialist leafhoppers are interactively affected by connectivity, landscape composition (complex or simple) and fragment size (large or small). Generalist leafhopper species richness increased with decreasing isolation in simple but not in complex landscapes and in small but not in large fragments.
According to our results, we assume that the specialists persist on the fragments of calcareous grassland without much exchange between them, especially because many species have limited dispersal abilities due to their short wings. Therefore, they do not seem to be affected by decreasing connectivity. In accordance with this result, Schuch, Wesche & Schäfer (2012) found no decrease in leafhopper species richness (but a marked decrease in abundance) in protected dry grasslands in eastern Germany over the last 50 years.
Generalist leafhoppers can be assumed to move more between fragments, especially because they are more likely to be long winged than specialists. However, the dispersal abilities of macropterous leafhoppers seem to be species dependent. In a mark and recapture experiment, Biedermann (1997) found that the froghopper Neophilaenus albipennis, even though able to fly, rarely moved more than 20 m from the original point of capture. Other leafhopper species are able to fly and bridge greater distances or get passively dispersed by air currents (Waloff 1973; Nickel 2003).
Despite being referred to as generalists here, a large proportion of the species recorded in this study require low-productivity habitats, that is, they cannot cope with the conditions that prevail in today's intensified agricultural landscapes. Only few species are able to breed in arable fields or intensified meadows and pastures, colonizing them anew every year (Nickel 2003). This leads to the assumption that calcareous grasslands are an important refuge for many leafhopper species, regardless of their degree of specialization. So where fragments of calcareous grassland are few and scattered, even these generalist species are likely to find it difficult to locate and subsequently colonize the next suitable fragment, explaining the decrease in generalist species richness with decreasing connectivity.
Increasing isolation caused a decrease in both overall and generalist leafhopper species richness in simple (high percentage of arable land) but not in complex landscapes. In simple landscapes, leafhoppers may find it difficult to reach the next suitable site, being unable to find suitable alternative resources or habitats with a similar vegetation type or structure during dispersal. Similar to our results, Baum et al. (2004) found that dispersal of the planthopper Prokelisia crocea depended on the surrounding matrix habitat (pure stands of Bromus inermis vs. mudflat). These contrasting matrices may be comparable to arable fields vs. more natural habitats. This implies that the permeability of simple landscapes dominated by arable land may be reduced compared with more complex landscapes (Eycott et al. 2012). The reduced permeability of the matrix may become more problematic with increasing distance between suitable habitat fragments and may explain the reduction in leafhopper species richness with decreasing connectivity in simple landscapes.
We found that generalist species richness increased with decreasing isolation in small but not in large fragments. In small fragments, a higher extinction rate due to stochastic effects in combination with a lower probability of recolonization with increasing isolation may cause the decline in generalist species richness (Hanski, Alho & Moilanen 2000). Recolonization of larger fragments is more probable (for a beetle species see Matter 1996), and fewer extinctions occur. Cronin (2003) found that immigration of the planthopper P. crocea into host plant patches decreased with decreasing patch size. Nevertheless, because distances between habitat patches were much lower (up to 50 m) than in this study, immigration was not limited by increasing isolation.
In contrast to our results, Krauss, Steffan-Dewenter and Tscharntke (2003) and Meyer, Gaebele and Steffan-Dewenter (2007) found a strong positive relationship between fragment size and species richness of butterflies, hoverflies and bees. Butterflies as well as hoverflies and bees have more complex habitat and resource requirements than leafhoppers. This appeared to be the reason why they need larger habitat fragments. Resource requirements of butterflies and bees change during their life cycle: adult butterflies feed on nectar, whereas the caterpillars feed on plant tissue (Ebert & Rennwald 1991). Bees require nectar and pollen, both as food for themselves, and to provision their brood cells, they need hollow or pithy plant stems, empty snail shells or cavities in the ground as nesting sites and nesting material like leaves, clay, small stones and plant resin (Westrich 1989). In other words, they need different resources that are often spatially separated. In contrast, leafhoppers lay their eggs directly onto the host plant and all life stages feed on plant sap, which is an ample resource throughout the growing season (Nickel 2003). This life-history strategy enables them to potentially stay on the same plant stem for all their life, which is likely to reduce the minimum fragment size required for persistence. Thus, the threshold for a decrease in generalist species richness with fragment size alone might not have been reached within the range of fragment sizes chosen for this study (smallest fragment: 0∙1 ha). It seems that many leafhopper species are able to cope with small fragment sizes as long as a sufficient amount of their host plant is present.
This is in accordance with Biedermann (1997) who showed a clear but species-dependent relationship between host plant patch size and the occurrence of three leafhopper species. So if a dispersing individual reaches the next fragment but the host plant patch is too small – which is more likely to be the case in small fragments – it will not be able to establish a stable population there, causing the lower species richness of specialists on small fragments we observed in this study.
Usually, a focus on large fragments is recommended (e.g. Krauss, Steffan-Dewenter & Tscharntke 2003), but according to our results, both large and small fragments deserve to be maintained because at least for generalist leafhoppers we found no generally negative effect of small fragment size, but only in combination with decreasing connectivity.
Plant species richness
Generalist leafhopper species richness increased with plant species richness on both connected and isolated fragments, but the increase was more pronounced on the connected ones. As mentioned above, leafhoppers live in close association with their host plants (Nickel 2003), spanning from strictly monophagous to highly polyphagous species (Nickel & Remane 2002). Host plants provide feeding resources, shelter and oviposition sites and are also used for the transmission of bioacoustic signals (Nickel 2003). We therefore assume that the more plant species occur per site, the more leafhopper species can occur because the appropriate host plant for more species will be provided. This finding is in accordance with Siemann et al. (1998) and Scherber et al. (2010) who found an increase in herbivore diversity when the number of plants in their experimental set-ups increased. So even if suitable plant resources are available, isolated fragments are less likely to be colonized than connected ones, resulting in an increase in leafhopper species richness with plant species richness that is less steep than the one on connected fragments.
Our results are the first to show not only that insect biodiversity on fragmented calcareous grasslands depends on habitat connectivity but that it is interactively affected by the four factors habitat connectivity, landscape composition, habitat area and plant species richness. Isolated fragments that are either small or located in simple landscapes are less likely to receive immigrants after extinction events, leading to a gradual reduction in species richness over time. These patterns should not only apply to leafhoppers but to other insect groups as well.
Mitigating the negative effects of habitat fragmentation therefore needs to take the surrounding landscape into account. Management should be prioritized towards increasing the connectivity (i) of small, isolated fragments, (ii) of fragments in simple landscapes and (iii) towards management efforts that enhance dispersal by increasing heterogeneity of both landscape composition and configuration. Moreover, extensive management of fragments by grazing or mowing, both relatively late in the season, to increase habitat quality for leafhoppers would benefit other insect groups as well.
We would like to thank Boris M Hillmann, Andrea Rösch, Éva M. Szegő and Felix Weiß for their help with data collection in the field. Sebastian Schuch gave an introduction into leafhopper identification to V.R. Urs Kormann, Lorenzo Marini, Herbert Nickel and Laura Sutcliffe provided helpful comments on earlier versions of this manuscript. Laura Sutcliffe helped to improve the English. We thank Nick A. Littlewood and one anonymous referee for their valuable comments. P.B. was supported by the Bolyai Research Fellowship of the Hungarian Academy of Sciences and by the German Research Foundation (DFG BA 4438/1-1). Financial support by the MWK graduate school ‘Biodiversität und Gesellschaft’ to V.R. is acknowledged.