Green Roofs and Pollinators (PDF)

www.nature.com/scientificreports OPEN Green roofs and pollinators, useful green spots for some wild bee species (Hymenoptera: Anthophila), but not so much...

www.nature.com/scientificreports OPEN Green roofs and pollinators, useful green spots for some wild bee species (Hymenoptera: Anthophila), but not so much for hoverflies (Diptera: Syrphidae) Jeffrey Jacobs *, Natalie Beenaerts & Tom Artois Urbanisation has become one of the major anthropogenic drivers behind insect decline in abundance, biomass and species richness over the past decades. As a result, bees and other pollinators’ natural habitats are reduced and degraded. Green roofs are frequently recommended as ways to counter the negative impacts of urbanisation on nature and enhance the amount of green space in cities. In this study we evaluated the pollinator (more specifically wild bees and hoverflies) diversity, abundance and species richness on twenty green roofs in Antwerp, Belgium. We analysed the influence of roof characteristics (age, surface area, height, percent cover of green space surrounding each site) on species richness or abundance of pollinators. In total we found 40 different wild bee species on the green roofs. None of the physical roof characteristics appear to explain differences in wild bees species richness and abundance. Neither could we attribute the difference in roof vegetation cover, i.e. roofs build-up with only Sedum species and roofs with a combined cover of Sedum, herbs and grasses, to differences in diversity, abundance, or species richness. We found a positive trend, although not significant, in community weighted mean body size for wild bees with an increase in green roof surface area. Roof wild bee communities were identified as social polylectic individuals, with a preference for ground nesting. Only eleven individuals from eight different hoverfly species were found. Our results show that green roofs can be a suitable habitat for wild bee species living in urban areas regardless of the roofs’ characteristics, but hoverflies have more difficulties conquering these urban green spaces. Urbanisation—the gradual shift in residence of the human population from rural to urban areas—combined with the overall growth of the human population causes an increase in habitat loss, more fragmentation and an overall change in habitat q ­ uality1. One of the major effects of this urbanisation trend is a serious threat to biodiversity on a global ­scale2,3. Increased city area results in species habitat loss, increased spatial distance between remaining pockets of green, and an overall change in habitat q ­ uality1. These factors have caused an overall decline in insect abundance, biomass and species r­ ichness4,5. Whether the rates of decline for insects are on par with or exceed those for other groups remains ­unknown6. Pollinators are no exception, and together with other functional insect groups also suffer from stressors such as parasites, pesticides and a lack of ­flowers7. Pollination is vitally important to ecosystems and crop production, with a staggering 87% (~ 310.000 species) of all flowering plants depending on animal p ­ ollination8. An annual market value of $235–577 billion worldwide, is directly attributable to animal ­pollination9. In the north-temperate zone (e.g. Europe) bees, hoverflies and lepidopterans dominate pollination, whereas, in other parts of the world other pollinators, such as wasps and beetles, may be just as ­important8. Domesticated honeybees are often used in agricultural areas, although wild bees are the more efficient p ­ ollinators10. In addition, the pollination service’s long-term stability is dependent on bee species richness and a­ bundance11,12. Global honeybee stocks have increased in the past fifty years, while wild bees appear to have declined substantially over this p ­ eriod7,13. The decline of pollinator species and their distribution is strongly influenced by habitat loss and fragmentation and is further magnified by global ­warming9. Although it is clear that urbanisation has an effect on pollinator abundance and species richness, the effects can go both ­ways14,15. Overall, lower pollinator species richness and UHasselt, Centre for Environmental Sciences, Agoralaan Gebouw‑D, 3590 Diepenbeek, Belgium. *email: jeffrey. [email protected] Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 1 Vol.:(0123456789)  www.nature.com/scientificreports/ abundance with a relative increase in the proportion of generalist pollinators, such as b ­ umblebees16 are associ- ated with an increase in ­urbanisation17,18. This is not necessarily a positive evolution, since specialist species appear to have superior pollinator effectiveness compared to generalist s­ pecies19, at least for some plant species. To counter the negative environmental effects of urbanisation and increase the total amount of green spaces in cities, the construction of green roofs is often ­promoted20. Green roofs can deliver several ecosystem services, such as benefits for water runoff and e­ vapotranspiration21. They are also an efficient solution to mitigate the heat island ­effect22 or increase habitat connectivity for mobile arthropod species by acting as stepping-stones between ­habitats23. In addition, green roofs can be suitable habitats for a wide variety of pollinator s­ pecies24–28. These roofs produce pollen and nectar throughout the summer and include a variety of nesting l­ ocations25,29. Furthermore, the increased insulation and hence warmer microclimate at roof level create favourable habitat conditions for some pollinator ­species30. However, plant–pollinator networks in urban environments have fewer plant–insect interactions than those in semi-natural h ­ abitats31. Urban settings have neutral or even positive effects on the biodiversity of several insect pollinator groups, particularly wild bee s­ pecies32. Possibly because they are more sensitive to agricultural pesticides than other ­groups33. Whether common species of wild bees such as Bombus terrestris (Linnaeus, 1758) are more or less abundant than some decades ago remains unclear. There are maps of past and present distributions of bees in well studied countries such as the United Kingdom, but little information is available on how populations have evolved over time in terms of a­ bundance7. Wild bees play a vital role in urban ecosystems as pollinators in gardens, parks, and other green s­ paces14,30,34, they respond to land-use change in a variety of ways, both within and between ­taxa35,36. Some habitats within cities support a high diversity of flowering plants and pollinating insects, although the shift to highly generalized habitats with less variation such as green roofs, may make pol- lination services in urban areas more susceptible to future disturbance e­ vents37. Extensive green roofs, which consist of a 5–20 cm deep layer of homogeneous, shallow, rocky substrate, are the most prevalent type of green roof in Europe. Allochthonous plants, such as species of Sedum or other drought-tolerant plants, are commonly used since they require little maintenance and are resistant to summer d ­ rought38. Plant and associated animal communities on green roofs are expected to become more diverse over time, as natural systems go through successive transitions marked by increasing d ­ iversity39. Arthropods and microorganisms start colonizing green roofs immediately, as they are typically carried in with planting material or ­substrate40,41. Wild bees use green roofs as a habitat on a regular b ­ asis24,25,28. There is, as expected, a positive impact on pollinator diversity and abundance on green roofs with an increasing diversity of entomophilous plant ­species25,28,29,42,43. Pollinator communities on green roofs are influenced by different green roof characteris- tics such as s­ ize42,44,45, ­height23,27, vegetation c­ over28,46 and the proportion of green space in the surrounding ­landscape25.The age of a green roof does not affect bee communities ­significantly28, although it affects abundance of other groups, such as ­Lepidoptera43, ­Collembola47 and spontaneous vascular plant ­richness48 in a positive way. Although correlations have been shown, the effects of urbanisation and green roof characteristics on pollinator communities are probably case-specific and differ between cities and climates. Hoverflies are gaining popularity as beneficial species and alternative managed pollinators due to their sig- nificant involvement in pollination and other ecological services. In Europe more than 70% of animal-pollinated wildflower species are visited by ­hoverflies49. However, hoverflies visiting green roofs have received far less atten- tion than wild bees. They depend on the availability of appropriate plant taxa such as Asteraceae and Crassulaceae for nectar and p ­ ollen50, and unlike bees they use the nectar as a source for ovarian ­development51. Hoverflies do not have a fixed home range and can transport pollen over greater distances than bees during ­foraging52. Moreover, during their larval development hoverflies are very restricted to specific microhabitats because of their ­diet53,54. Due to their specific ecology hoverflies need a variety in landscape characteristics. Hoverflies require both suitable habitats for their larvae and flower resources at landscape scales; however, due to dispersal, habi- tat fragmentation, and barriers in built structures (e.g. large buildings), such resource complementarity is less common in urban a­ reas55. Previous studies have shown that the small number of ideal habitats in urban areas is probably the main cause of the higher sensitivity of hoverflies to urbanisation compared to b ­ ees55,56. Further- more, size and morphology can have an impact on pollinator efficiency and determine the amount of pollen the hoverfly can ­carry54. Individuals’ spatial scale at which they perceive their world is influenced by their dispersal capabilities. Hoverfly species can disperse anywhere from a few meters to 2 kms every ­day57,58, but most species only disperse over very short distances, except during mass migration events. The aim of our study was to investigate whether roof characteristics influenced pollinator diversity, abundance and species composition of green roofs in an urban environment. Therefore, we investigated 20 large green roofs in the city of Antwerp, Belgium. More specifically we expected that (i) green roofs with a large surface area would have a higher pollinator richness, abundance and diversity. We analysed (ii) if other roof characteristics (e.g. height) influenced species richness, abundance or diversity of pollinators present. Furthermore, we hypothesised (iii) that green roofs with a greater floral richness, i.e. here having a mixed vegetation cover of Sedum, grass and herbs, have a higher diversity and abundance of pollinators than the Sedum monoculture roofs. Finally, we analysed community weighted means to determine the average community traits (body size, social behaviour, flower visiting and nesting type) of wild bee species on the green roofs. We compared these CWM results for the two main roof types (Sedum vs Sedum/herbs/grasses), as species use traits to maximize their fitness in a different environment. Materials and methods Study sites. Our study areas comprised 20 green roofs in the city of Antwerp, Belgium. The city of Antwerp (51° 13′ N, 4° 24′ E) comprises a total area of 204.5 ­km2 with ± 526.000 citizens (2413.1 inhabitants/km2). We sampled macro-invertebrates from the months of March until September in the years 2020 and 2021. Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 2 Vol:.(1234567890) www.nature.com/scientificreports/ The average temperature during the sampling period of 2020 was 15.3 °C (± 0.1) and the average precipitation was 53.6 ­mm59. From August 5–16 2020 a heatwave occurred (i.e. the temperature was at least 25 degrees on five consecutive days or more, with at least 30 degrees being reached for three days;59). The average temperature during the sampling period of 2021 was 14.7 °C (± 0.1) and the average precipitation was 91.6 mm. During the months of June (121 mm), July (166.5 mm) and August (123 mm) 2021 the precipitation exceeded the overall averages of these months (June: 70.8 mm, July: 76.9 mm and August: 86.5 mm)59. The percentage of grassland in the surrounding landscape within a radius of 300 m centred at the middle of each green roof was calculated using the software Google Earth Pro (version 7.3.6.9345) (see appendix table A7 and figure A6 in supplementary information). Green roof characteristics. On average the green roof surface was 280.6 m ­ 2 (range 8 m ­ 2–896 ­m2), the average age was 8.4y (range 3–14y), and their average height was 10.4 m (range 4–23 m; Table 1). The roofs are made up of a 5–20 cm layer of homogeneous, shallow rocky substrate. They are typically planted with species of Sedum or other drought tolerant plants (e.g. species of mosses and grasses such as Calamagrostis epigejos (Roth, 1788)). Roofs were separated into two groups according to the vegetation type Sedum roofs (Mid 1, Mid 2, Onyx, Eco 1, PM, RSL, RPBer, RPDeu, Iglo, Bell, Arena) and Sedum, herbs and grass roofs (Dis, Atlas, Eco 2, Ell, Hard, Bra, RPWil, Boek 1, Boek 2). We conducted two vegetation surveys on all roofs in June 2020 and 2021 (see appendix table A3 in supplementary information for an overview of the flora species per green roof). Data collection. We sampled the green roofs every three weeks from March till September 2020 and 2021 to assess flying invertebrate biodiversity with randomly installed pan traps (diameter = 12 cm, height = 4 cm) of four different colours (blue, yellow, red and white;60). The pan traps were filled with clear propylene glycol and were emptied after 24 h. Invertebrates were stored in 70% ethanol. We also sampled the green roofs with the use Name roof Reference Location Age (y) Surface ­(m2) Height (m) Dominant vegetation Antwerpen (N51.184°, Middelheim 1 Mid 1 7 260 10 Sedum E4.420°) Antwerpen (N51.184°, Middelheim 2 Mid 2 7 45 10 Sedum E4.419°) Berchem (N51.193°, Onyx Onyx 7 708 23 Sedum E4.417°) Wilrijk (N51.169°, District Dis 13 320 9 Sedum, herbs and grasses E4.394°) Antwerpen (N51.130°, Atlas Atlas 8 320 8 Sedum, herbs and grasses E4.253°) Borgerhout (N51.125°, Ecohuis 1 Eco 1 3 35 12 Sedum E4.260°) Borgerhout (N51.125°, Ecohuis 2 Eco 2 3 8 12 Sedum, herbs and grasses E4.260°) Antwerpen (N51.218°, Plantin Moretus museum PM 5 84 15 Sedum E4.398°) Antwerpen (N51.230°, Ellerman Ell 6 312 9 Sedum, herbs and grasses E4.415°) Antwerpen (N51.135°, Hardenvoort Hard 5 630 20 Sedum, herbs and grasses E4.251°) Antwerpen (N51.135°, Red Star Line museum RSL 10 408 10 Sedum E4.241°) Antwerpen (N51.251°, Brandweer Bra 12 777 17 Sedum, herbs and grasses E4.418°) Wilrijk (N51.160°, Recycling park Wilrijk RPWil 7 164 4 Sedum, herbs and grasses E4.390°) Berchem (N51.194°, Recycling park Berchem RPBer 7 154 4 Sedum E4.439°) Deurne (N51.237°, Recycling park Deurne RPDeu 7 142 4 Sedum E4.457°) Urban childcare centre Antwerpen (N51.225°, Iglo 9 896 5 Sedum Strandloper E4.380°) Administrative centre Antwerpen (N51.205°, Bell 12 85 21 Sedum den Bell E4.399°) Deurne (N51.197°, Boekenberg park 1 Boek 1 14 108 5 Sedum, herbs and grasses E4.463°) Boekenberg park 2 Boek 2 Deurne (N51.197°, E4.462) 14 85 4 Sedum, herbs and grasses Deurne (N51.199°, OCMW Arena Arena 13 72 6 Sedum E4.459°) Table 1.  Overview of the roofs with their reference name, age, surface area, height above ground level and dominant vegetation. Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 3 Vol.:(0123456789)  www.nature.com/scientificreports/ of pitfall traps (diameter = 8 cm, height = 6 cm) to assess ground dwelling macro-invertebrate ­biodiversity61,62. We installed four pitfall traps at each site at random. The pitfall traps were covered with a lid to protect the trap from flooding with rain, and again propylene glycol was used to fill the traps to capture the i­nvertebrates63. Every three weeks traps were emptied and invertebrates were preserved in 70% ethanol. All wild bee speci- mens were identified to species l­evel64 and validated by experts Mr. Jens D’Haeseleer and Mr. Win Vertommen (Natuurpunt Studie-Mechelen) (Identification of the Bombus terrestris-group is difficult, because many Bom- bus species are cryptic and morphological identification may be impossible between the four different species: Bombus terrestris, Bombus magnus, Bombus lucorum and Bombus cryptarum65). Wild bee traits were categorised and ­identified64,66,67. Hoverflies were identified to species ­level68 and identification was confirmed by Mr. Ward Tamsyn (Natuurpunt Studie-Mechelen) and Mr. Guy Van de Weyer. Honeybees (Apis mellifera) were excluded as they are domesticated bees depending on manmade hives. Statistical analysis. Community diversity measures for wild bees were quantified for each roof (data was pooled across the season for each roof), including species richness, abundance, Shannon–Wiener’s index (H′), inverse Simpson’s diversity index (D), and Pielou evenness (E). To determine whether the respective meas- ures were significantly different between green roofs, Poisson generalized linear mixed models (GLMM) were applied, as Poisson distribution is typically used for count ­data69. Green roof characteristics (vegetation type (categorical), age (continuous), height (continuous), surface area (continuous), percentage of grassland in the surrounding area (continuous)) were used as the fixed factors, roof as the random factor, and each diversity measure (richness, abundance, H′, D, E) as an independent variable. A penalized quasi-likelihood approach was used as a lognormal distribution best fits all responses. Community weighted mean (CWM) trait values for each individual roof were calculated for body size, social behaviour, flower visiting and nesting of wild bee species. The difference in CWM (body size, social behaviour, flower visiting and nesting) values between Sedum roofs and Sedum/herbs/grasses roofs were checked performing sample paired t tests. All data were analysed using R version 3.6.370, and the packages: “vegan”71, “matrixStats”72, “lme4”73 “dplyr”74 and “MASS”75. Results Wild bees. In total we collected 597 individuals belonging to 40 different species (Table 2). The average number of species per roof was 8 (x̄ = 7.6, sd = 4.9); roofs housed between two and eighteen species. The number of wild bee individuals sampled per roof varied from three to 168 (x̄ = 29.85, sd = 36.8). The most abundant spe- cies were Lasioglossum laticeps, Bombus terrestris-group and Hylaeus hyalinatus (Table 2). Some species such as Lasioglossum morio were found on all roofs except four (Onyx, Ell, Eco 2 and Dis). In contrast, twenty species were only found on one roof such as Andrena cineraria or Lasioglossum semiculens (See Appendix Table A1 in supplementary information). Most of the individuals (521) were caught with the use of pan traps; only a relatively small number (76 individuals) were caught as by-catch from the pitfall traps. The yellow pan traps attracted the highest numbers (303), while the red pan traps attracted the least individuals, only six (See appendix figure A2 in supplementary information) (Fig. 1). Wild bee diversity, species richness and abundance. GLMM results show no significant differ- ences in abundance, species richness and any of the diversity indices between roofs made up of only Sedum species and roofs with a combined vegetation cover of Sedum, herbs and grasses (Table 3). No significant dif- ferences were found when analysing the effect of roof characteristics such as the height, age (i.e. time since construction),surface area and proportion of grassland in the surrounding landscape on the species richness and abundance nor when comparing the two sampling years (Table 4). Community weighted means of wild bee traits. Bee communities are composed of bee species with certain traits, the typical trait value within the communities for social behaviour (CWM;76) indicates that the average wild bee communities on the green roofs are social (see appendix Table A4 in supplementary informa- tion).The average bee communities on the green roofs prefer ground nesting. Most species found in this study are polylectic (35 species, abundance 98.9%). Only a small minority of five oligolectic species were found (abun- dance 1.1%; Table A4). The average CWM for body size ranged between 4.00 mm and 9.75 mm (Table A4). Our results show that wild bee body size does not increase nor decrease significantly with an increase in green roof ’s height (See appendix figure A3 in supplementary information). Although statistically not significant (p-value = 0.097), we found a positive trend in CWM average body size with an increase in surface area of the green roof (see appendix figure s4 in supplementary information). Comparison of the two types of roofs (Sedum vs Sedum/herbs/grasses) via dependent sample t-tests showed no significant differences in CWM values (social behaviour: p(0.979), nesting: p(0.796), flower visit: p(0.139) and body length: p (0.441)). Hoverflies. In total we collected 11 hoverfly individuals from eight different species during the entire sam- pling period (See appendix Table s5 in supplementary information). All individuals were caught with pan traps. This very low number of individuals allows for no further statistical analysis due to the sample size being too small and increasing the margin of error significantly. Hence, we are unable to include the hoverflies in our further hypothesis testing. Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 4 Vol:.(1234567890) www.nature.com/scientificreports/ Family Genus Species Abundance Andrenidae Andrena barbilabris (Kirby, 1802) 1 Andrenidae Andrena cineraria (Linnaeus, 1758) 1 Andrenidae Andrena dorsata (Kirby, 1802) 1 Andrenidae Andrena minutula (Kirby, 1802) 2 Andrenidae Andrena nitida (Müller, 1776) 3 Andrenidae Panurgus calcaratus (Kirby, 1802) 1 Apidae Anthophora quadrimaculata (Panzer, 1798) 1 Apidae Bombus hortorum (Linnaeus, 1761) 2 Apidae Bombus lapidarius (Linnaeus, 1758) 27 Apidae Bombus pascuorum (Scopoli, 1763) 55 Apidae Bombus terrestris-group* 102 Apidae Nomada fabriciana (Linnaeus, 1767) 2 Apidae Bombus vestalis (Geoffroy, 1785) 2 Colletidae Colletes daviesanus (Smith, 1846) 1 Colletidae Hylaeus communis (Nylander, 1852) 3 Colletidae Hylaeus hyalinatus (Smith, 1842) 85 Colletidae Hylaeus pictipes (Nylander, 1852) 5 Halictidae Halictus rubicundus (Christ, 1791) 2 Halictidae Halictus scabiosae (Rossi, 1790) 1 Halictidae Lasioglossum fulvicorne (Kirby, 1802) 5 Halictidae Lasioglossum laticeps (Schenck,1870) 103 Halictidae Lasioglossum leucopus (Kirby, 1802) 1 Halictidae Lasioglossum leucozonium (Schranck, 1781) 2 Halictidae Lasioglossum lucidulum (Schenck, 1861) 1 Halictidae Lasioglossum minutissimum (Kirby, 1802) 1 Halictidae Lasioglossum morio (Fabricius, 1793) 84 Halictidae Lasioglossum nitidulum (Fabricius, 1804) 52 Halictidae Lasioglossum pauxillum (Schenck, 1853) 1 Halictidae Lasioglossum semilucens (Alfken, 1914) 1 Halictidae Lasioglossum sexstrigatum (Schenck, 1870) 2 Megachilidae Anthidium manicatum (Linnaeus, 1758) 4 Megachilidae Chelostoma rapunculi (Lepeletier, 1841) 2 Megachilidae Coelioxys rufescens (Lepeletier & Serville, 1825) 1 Megachilidae Megachile centuncularis (Linnaeus, 1758) 1 Megachilidae Megachile ericetorum (Lepeletier, 1841) 1 Megachilidae Megachile rotundata (Fabricius, 1787) 24 Megachilidae Megachile willughbiella (Kirby, 1802) 1 Megachilidae Osmia bicornis (Linnaeus, 1758) 5 Megachilidae Osmia caerulescens (Linnaeus, 1758) 1 Melittidae Dasypoda hirtipes (Fabricius, 1793) 7 Table 2.  Overview of wild bee species found on the green roofs (*B. terrestris-group: Bombus terrestris (Linnaeus, 1758), Bombus lucorum (Linnaeus, 1761), Bombus magnus (Vogt, 1911) and Bombus cryptarum (Fabricius, 1755). Abundance: number of individuals caught during the whole sapling period)). Discussion With biodiversity loss occurring at an unprecedented ­rate77 and urbanisation increasing globally, there is an urgent need to optimize urban areas to support biodiversity increase and its ecosystem services, with pollination being a vital one. In this study we explored how green roof characteristics influence the diversity, abundance and species richness of wild bees on these roofs. Our findings can be used to support future biological landscape planning on roofs to optimise pollinator abundances, species composition and diversity in urban areas. The studied green roofs hosted 40 wild bee species, which represents around 10% of Belgium’s 403 recorded ­species78 and reflects the typical species richness documented globally for studies on green roofs i.e. ranging between 17 and 90 s­ pecies25–29,46. Our findings did not support our first hypothesis being green roofs with a large surface area have a higher wild bee species richness, abundance and diversity. Larger roofs did not show a positive or a negative effect on species abundance or richness of wild bees (Table 4). It is known that a large number of small green patches, represented by green roofs here, can accumulate species richness even more than a few large patches with an equal total Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 5 Vol.:(0123456789)  www.nature.com/scientificreports/ Figure 1.  Diversity indices two years combined for each green roof (Shannon–Wiener diversity index: blue bars; Simpson diversity index (inverse): orange bars; Pielou evenness: grey bars). Estimate SE Z-value P-value Abundance 0.042 0.532 0.064 0.842 Species Richness 1.567 2.214 0.664 0.423 H’ 0.078 0.274 0.105 0.811 D 0.034 0.063 0.535 0.899 E 0.017 0.046 0.284 0.674 Table 3.  GLMM results of the fixed factor for abundance, species richness and the diversity indices (Shannon Wiener: H′, Simpson: S and Pielou’s Evenness: E) between green roofs with a vegetation cover of Sedum only and green roofs with a with a mixed vegetation cover of Sedum, grass and herbs. Table shows the estimate, standard error (std. Error), Z-value and p-value. Estimate SE Z-value P-value a) Abundance Age -0.026 0.068 -0.382 0.603 Height -0.045 0.043 -1.051 0.293 Surface area 0.016 0.001 0.538 0.591 Proportion grassland 0.002 0.034 0.065 0.948 Comparing two years 1.34 6.423 0.241 0.786 b) Richness Age 0.583 0.446 1.307 0.246 Height -0.023 0.004 -0.525 0.428 Surface area -0.003 0.004 -0.809 0.418 Proportion grassland 0.001 0.004 0.445 0.656 Comparing two years 0.046 1.456 0.038 0.964 Table 4.  Fixed effects table for the generalized linear mixed model (GLMM) detected in the green roof samples for abundance (a) and richness (b) of wild bees (and comparing the two sampling years). Table shows the estimate, standard error (std. Error), Z-value and p-value. Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 6 Vol:.(1234567890) www.nature.com/scientificreports/ habitat ­area79. As a result, it is important to urge the public to install green roofs, even those with smaller roofs, as these can be evenly beneficial in terms of wild bee species richness than large green roofs. Our results show a slight positive effect on the average body size of wild bee species with an increasing surface area (see appendix figure s4 in supplementary information), but there remains a huge information gap about how urbanisation influences body size changes in wild bee communities and the mechanisms behind ­these80. Furthermore, the findings of our study indicate that the percentage of grassland in the surrounding area has no significant effect on wild bee species abundance or richness on the sampled green roofs (Table 4). This result aligns with a previ- ous study which found that grassland in the surrounding area did not have an impact on arthropod diversity and ­richness81. Additionally, the majority of the green space surrounding our green roofs consists of turf grass, which has been shown to have no significant effect on abundance or diversity of wild bee species on green roofs ­before25. However, with studies that have yielded varying results, it remains uncertain as to the extent to which the surrounding green space impacts the arthropod communities found on green roofs. Increasing roof height did not affect wild bee abundance nor species richness. When testing for an effect of green roof height on body size, we again could not find any differences. Probably the height of our roofs is not distinctive enough for the wild bees to distinguish for these metrics. Moreover, small variations in vegetation appear to have an effect on the fauna ­present82. We only used roofs reflecting the two most popular types around the world i.e. roofs covered with Sedum species only and roofs covered with a combination of Sedum, herbs, and grasses, but could not detect significant differences in abundance, species richness or any of the diversity indices of wild bees (Table 3) between both types. Indecisive whether the vegetation plays a role in it, the bee communi- ties on the green roofs were dominated by social species (29 species; Table A4). While some research shows that social bee species are more abundant in urban a­ reas83,84, others show that solitary bees are more common in those ­areas85. Our results further add to the findings that the occurrence of this trait is case-specific regarding meth- odologies and areas of research used in different s­ tudies86, moreover, the variation in reaction among different bee species to urbanisation adds to this discrepancy. Green roofs in our study seem to be a suitable habitat for ground nesting species in an urban environment (table A4) contrasting the findings that above-ground nesting wild bee species are typical for urban a­ reas86,87. The latter is probably due to the presence of a higher number of potential nesting s­ ites88. Ground-nesting bees are probably less frequently found in urban areas due to the limi- tation of suitable nesting sites, the strong human disturbance and their sensitivity to habitat fragmentation. On top of that bare soil patches typically disappear in urban landscapes. On green roofs these patches are typically more present. This study, however, does not allow us to claim that the bees are effectively nesting on the roofs. The bees sampled on our roof could reflect bees that nest in the surrounding landscape and use the roof top as a foraging habitat patch, or bees that nest in the roof and forage on flowers on the roof (or in the surrounding landscape), or bees opportunistically foraging from our pan traps. A previous study on wild bees in the city of ­Antwerp89 also showed a light preference for ground-nesting. However, these results can be explained by the fact that the bee sampling was performed in gardens, parks and cemeteries, where free (undeveloped) soils were still available. It is likely that these places, together with green roofs, act as sanctuaries for ground-nesting wild bee species in an urban environment. The relatively high abundances of Lasioglossum morio and Lasioglossum laticeps (Table 2) were rather expected as they are quite prevalent in urban settings, including urban green ­roofs28,90,91. Furthermore, other species, such as Lasioglossum sextrigatum, Hylaeus hyalinatus, Osmia bicornis, Anthidium manicatum, Anthophora quadrimaculata, Megachile centuncularis, Dasyopoda hirtipes, sampled in this study are also positively associated with urban areas in our r­ egion92. Lasioglossum species are typically regarded as less efficient pollinators compared to honeybees and ­bumblebees93, due to their smaller body s­ ize94,95, carrying capacity to transfer pollen grains to s­ tigmas96, and their slower movement between flowers. However, due to their large numbers they are still considered as effective ­pollinators93,94,97. Until now Lasioglossum morio is known as the only wild bee species that can spend its whole life cycle on green r­ oofs98. Interestingly, genera such as Lasioglossum appear to be more resilient than other genera, such as Andrena, to land-use ­change99, however, other findings show negative effects on Lasioglossum species abundance with greater u ­ rbanisation100. These varying effects of urbanisation can also be seen in the abundance 101,102 of ­bumblebees. Although we did not study green roofs in less urbanized environments, our findings sug- gest that Lasioglossum and Bombus abundances are at least not negatively impacted by urbanisation (Table 2). Urbanisation in Europe is causing the decline of specialized s­ pecies103. In general bee communities on our green roofs are made of polylectic species and less of oligolectic species (see appendix table A4 and table A2 in supplementary information), as a broader diet is likely best for facilitating species expansion in urban ­areas25,104–106. The specific diet of oligolectic species is rather difficult to maintain in urban settings due to the lack of sufficient plant species to collect pollen. Furthermore, the retrieval of only a few cleptoparasitic species (Bombus vestalis, Ceolioxys rufescens and Nomada fabriciana) corresponds to the findings of Braaker et al.107 and Passaseo et al.108. Our findings thus indicate that green roofs primarily harbour generalist species rather than specialist species with a higher pollinator effectiveness. Although our main study objectives focus on wild bees, we share some brief findings on our hoverfly samples. Only 11 hoverfly individuals belonging to eight different species were discovered (See appendix table s5 in supple- mentary information). Hoverflies occur only in very low diversities and abundances in urban ­environments56,109, including on green r­ oofs108,110,111. The lack of sufficient plants, aphids, and decomposing vegetal debris in urban contexts possibly creates a scarcity of larval food supplies. The homogeneous landscape also provides less egg laying sites, making it difficult for species to complete their whole life ­cycle56. Four out of the eight species found (Episyrphus balteatus, Melanostoma mellinum, Scaeva pyrastri and Sphaorphoria scripta) are in fact strong migra- tory ­species112,113 with less difficulties conquering the habitat isolation of green roofs. Moreover, E. balteatus, S. pyrastri and Merodon equestris are highly anthropophilic species and Helophilus pendulus, S. scripta and M. mel- linum are species regularly found in urban or suburban h ­ abitats67,112. Furthermore, S. scripta is known to be one of the few hoverfly species capable of spending their whole life cycle on green ­roofs98. Although it is challenging Scientific Reports | (2023) 13:1449 | https://doi.org/10.1038/s41598-023-28698-7 7 Vol.:(0123456789)  www.nature.com/scientificreports/ to draw any conclusions from our results due to the extremely small sample size, our findings indicate that only few hoverflies use green roofs as a suitable habitat. It is incomprehensible that so little research has been done on hoverflies on green roofs or in urban settings in general, when you know that more than 70% of animal- pollinated wildflower species are visited by hoverflies. Future research should in our opinion, move away from concentrating just on honeybees and bumblebees, and instead involve this significant pollinator group more. Our sampling methodology might have caused some bias in hoverfly and bee observations. Some species, such as Bombus, are less commonly caught in pan t­ raps114. The integration of active netting together with pan trapping is often suggested as a possible solution for a more exhaustive sampling method of bee and hoverfly populations. However, active netting over multiple sampling sites is extremely labour-intensive for only a single person to sample in the same time frame to ensure for instance similar weather conditions. There is also a large risk in creating additional biases by the sampler and sampling moment if more samplers or different times are used. As discussed above, green roofs vary depending on their surrounding environment, vegetation cover, height, age, and a variety of other factors. As a result, and due to the large heterogeneity in urban areas, it remains difficult to identify explicitly the true drivers behind our findings and to compare one on one different green roof stud- ies. As mentioned before, the effects of urbanisation on pollinator communities are probably case-specific and differ between regions and climates. Future studies should seek to minimize variability in sampling techniques, study periods, and other methodological differences that may underlie inconsistent results and conclusions. Overall, our results indicate that green roofs in Belgium can be a habitat for a variety of wild bee species in an urban environment. 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The author J.J. and the research was funded by the SBO project ‘Ecocities: Green roofs and walls as a source for ecosystem services in future cities’, S002818N. The author J.J. was supported by the Special Research Fund: BOF21DOC24. Author contributions J.J. is responsible for conceptualization, methodology, formal analysis, investigation, data curation, writing— original draft, visualization and the resources. While both authors N.B. and T.A. are joint supervisors and responsible for writing—review & editing, supervision and funding acquisition. Competing interests The authors declare no competing interests. Additional information Supplementary Information The online version contains supplementary material available at https://​doi.​org/​ 10.​1038/​s41598-​023-​28698-7. Correspondence and requests for materials should be addressed to J.J. Reprints and permissions information is available at www.nature.com/reprints. 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