Importance of vegetated roofs for arthropods
We studied arthropod assemblages on different kinds of urban vegetated roofs to evaluate their habitat and conservation value, and to find roof designs that best promote these targets. The main local drivers of arthropod abundance across a variety of urban succulent to meadow roofs were vegetation type and roof height. The roofs hosted mainly common open and semi-open habitat species, lacked species of conservation concern, and may have introduced non-natives. The orders/suborders we collected from the roofs reflected suction sampling data from urban ground level open habitats (Bolger et al. 2000; Kutschbach-Brohl et al. 2010). Yet, the absence of grasshoppers (Orthoptera) was surprising. The likely explanations are their sensitivity to fragmentation (Appelt and Poethke 1997) and the sampling method we used. The combination of small patch size and isolation from source habitats may prevent grasshoppers from establishing populations on the studied roofs. Moreover, although grasshoppers are better caught with sweep netting compared to vacuum sampling, vacuuming line transects do yield grasshoppers (Doxon et al. 2011), but vacuuming several circle-shaped spots may give these highly visual animals better chances to escape. In summary, we did not find support for arthropod communities on vegetated roofs being species rich or including rare or endangered native species, an argument often applied to promote vegetated roofs. However, the roofs we studied were not specifically built for conservation purpose and may thus lack key qualities that promote habitat provision for arthropods. Thus, it would be interesting to design test roofs specifically for conservation purposes to explore their capacity to attract and support declining, rare and endangered species.
We collected one true bug species new to Finland (C. evanescens), which is widely distributed in Central and Southern Europe and feeds on sedums (Linnavuori 2007). The species has also been found on vegetated roofs in London, where it is classified as nationally rare (Jones 2002). Jones (2002) argued that it had likely arrived with pre-grown imported succulent mats, a probable explanation also for the presence of C. evanescens on two of our study roofs. If brought with roof materials, it must have overwintered and reproduced on the roofs several times, as these roofs were three years old.
Previously, vegetated roofs established with prefabricated succulent mats in Helsinki have also been found to host two snail species rare in Finland (Páll-Gergely et al. 2014), and a black fungus gnat species (Diptera, Sciaridae) new to the country (Pekka Vilkamaa, Finnish Natural History Museum, personal communication). Rather than supporting the idea of vegetated roofs as effective tools for arthropod conservation, the presence of these locally rare species raises a concern about species introductions. Imported plant material is globally recognized as a major pathway for invasive insects, and constructed habitats are among the most important outdoor habitat types for alien insect species (Kenis et al. 2007). The risk for species introductions is likely to be higher on roofs that are built using imported prefabricated vegetation mats, compared to roofs established with plug plants and seeds. Yet, as we lack direct evidence on the origins of these species, this topic requires further investigation.
Spider, true bug and ant communities on the roofs
Spider communities were dominated by one common and highly dispersive pioneer species, and the number of species per roof was typically low (most roofs had < 5 species). Also, the total number of spider species in our data (23 on 17 roofs) was low compared to studies on vegetated roofs in other climates and with different collection methods (Brenneisen and Hänggi 2006; Braaker et al. 2014; Bergeron et al. 2018). Spider communities did not differ statistically significantly between roof types. Yet, this seems to be explained by large differences in community composition within each roof type, rather than by similarity of communities on different types of roofs (see Fig. 2c). Moreover, the dominance of the highly dispersive Linyphiidae-family indicates that roofs are frequently re-colonized. Brenneisen and Hänggi (2006); Bergeron et al. (2018) also found Linyphiidae to be among the most frequent spiders, but not always dominant. Finally, the low abundance of Lycosidae (wolf spiders) was surprising, because they are typical of open habitats (Jocqué and Alderweireldt 2005) and also found on vegetated roofs (Brenneisen and Hänggi 2006; Braaker et al. 2014; Bergeron et al. 2018). It may be that our roofs were too small for hunting spiders requiring larger space compared to web-weavers, or that our collection method did not capture hunting spiders efficiently (see “Limitations of the study”). At least Bergeron et al. (2018) studied mostly roofs that were larger than ours (their roof size varied from 221 m2 to 825 m2), supporting our size-limitation explanation.
The true bug communities on succulent roofs were different from those on the two other roof types, which indicates that plant assemblages shape true bugs at the family level. According to trait data, true bug communities are characterized by herbivores that are associated with dry open habitats, dwell on the ground and/or in the herb layer and overwinter either as eggs or adults. We did not collect fully short-winged species, but found short-winged individuals of polymorphic species. Because short-winged individuals are unlikely to colonize roofs by themselves, they are probably offspring of long-winged individuals, or of short-winged individuals that arrived with roof materials. Almost all herbivorous true bugs were generalists (oligo- or polyphagous), which is typical for urban fauna (Knop 2016), but also supports the idea of Lundholm and Walker (2018) that vegetated roofs hardly match the requirements of highly specialized species unless specifically designed to do so. The number of true bug species per roof was low, but the total number of species was higher than reported in any previous studies. Yet, the comparability to previous studies is feeble as they are scarce and used various methods (suction sampling, Jones 2002; pitfalls, MacIvor and Lundholm; hand sampling, Madre et al. 2013).
Ant communities are usually species rich in urban areas (Santos 2016), with efficiently dispersing pioneer species and habitat generalists overrepresented as compared to rural areas (Vepsäläinen et al. 2008). The two species found on our study roofs, L. niger and M. rubra, are indeed generalists and also the most common species in the Helsinki area, and common in other European cities as well (Vepsäläinen et al. 2008). The observed increase in ant abundance with substrate depth and dead plant material is logical, because both species nest underground (Collingwood 1979), and litter helps the soil to hold moisture, making nest excavation easier. Ant species richness has been suggested to indicate the ease of colonization of new areas in urban environments (Yamaguchi 2004), the low number of species here pointing towards low accessibility.
Impact of roof characteristics on individually analyzed taxa
Results of the GLMMs supported only few of the hypothesized patterns but suggested other effects of roof characteristics on arthropods. The positive response to dead plant material was in line with the literature: litter creates shelter and positively affects predators by increasing prey abundances (Bultman and Uetz 1982). In contrast to Kyrö et al. (2018), roof age was unimportant in shaping arthropod abundance and it had both positive and negative effects when retained in the final models. Age was correlated with grass cover (r = 0.88) and because the effect of grass was mainly negative, it is likely that an increase in grass cover on older roofs decreases abundances of most arthropod taxa. Thus, roof age itself does not seem to affect arthropod abundance, but it has indirect effects via changes in vegetation.
Contrary to our hypothesis and previous findings with negative (Madre et al. 2013; MacIvor 2016) or varying effects (Kyrö et al. 2018) of roof height on the abundance of arthropods, our results support a positive effect of height on abundance. We found no effect of height on species richness, while previously height has been found to have positive, yet weak, effects on richness (Blank et al. 2017, based on Kadas 2006 data). Blank et al. (2017) suggested that weak and varying height effects are explained by low number of replicates and that positive height effect on richness is likely to be related with correlations between height and other roof variables, particularly roof size. In our data, height showed low collinearity (VIF < 3) with other continuous variables and height frequently remained in the final models for arthropod abundance. The highest roof in our data was 11 m, which is low compared with most previous studies (reviewed in Blank et al. 2017). Thus, the positive height-abundance connection we found may not hold on very high roofs. However, current evidence indicates that height does not limit the value of roof environments for a majority of arthropods that are able to colonize roofs. The mostly positive response to roof height could be related to decreased competition or predation on high roofs, but further studies are needed to be able to assess the role of biotic interactions on vegetated roofs.
The effect of roof size on arthropod abundances appears to vary (Madre et al. 2013; Ksiazek-Mikenas et al. 2018; Kyrö et al. 2018), and even though we found a positive size effect on true bug diversity, size does not seem to be important in explaining arthropod diversity on vegetated roofs in general (Madre et al. 2013; Braaker et al. 2014, 2017). A likely explanation is the small-island-effect (SIE), where species richness varies independently of patch area up to a certain minimum threshold value (Lomolino 2000). Even the largest roofs (350 m2 in our data) are below the estimated threshold for SIE for invertebrates (Wang et al. 2018).
We showed that arthropod communities differ between succulent, succulent-meadow and meadow roofs. Though we found no effect of the number of plant species on arthropod species richness, the ordinations still suggested that plant diversity had a community level impact on arthropods. Spiders, beetles and some true bugs showed negative abundance responses implying that they are more abundant on plant species-poor succulent roofs than species-rich meadow roofs. A positive relationship between succulent cover and arthropod abundance was also shown by Kadas (2006) comparing succulent and brown roofs in London. The vegetation on brown roofs relies on spontaneous colonization and the seed bank in the substrate, and they are expected to have a diverse vegetation. Kadas (2006) explained the result by the correlation of vegetation type and roof age (brown roofs were only one year old while the age of succulent roofs varied). However, our finding cannot be explained the same way, as many of our succulent roofs were younger than our meadow roofs, yet all roofs were at least three years old.
Finally, our hypothesis that roof size and height are more important to predatory arthropods than herbivores, was supported by the ordinations, where spider communities (the only fully predatory group in our data) were shaped by both vegetation characteristics and roof size and height at the family level, whereas (mainly herbivorous) true bug communities were only shaped by vegetation characteristics. However, the GLMMs did not support this hypothesis as, on one hand, vegetation variables were important also in shaping spider abundances and, on the other hand, true bug abundances were shaped by both vegetation characteristics and roof height.
Limitations of the study
Our study is among the first to vacuum sample arthropods on vegetated roofs. Thus, differences in our data compared to previous studies can partially be explained by the sampling method. The advantage of vacuum sampling is that substrate depth does not limit the selection of roofs, as it does for pitfall trapping. D-vac efficiently captures small, ground-dwelling and epiphytic arthropods, but is not optimal to collect large and heavy species or those that hide in the ground or under stones, such as Lycosidae spiders (Mommertz et al. 1996; Doxon et al. 2011; Standen 2000). It also only gives a snapshot of the fauna, while the air current, accompanied with loud engine noise, likely affects capture.