Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan

Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan Our study provides a first look at the relationship between large-scale buildings incorporating vegetation (Dense and Green) and bird species richness in Milan, and is one of the studies conducted so far to assess this relationship globally. We carried out our survey in and around three Dense and Green and six high-density buildings with no vegetation (Normal Dense). Dense and Green buildings had a higher mean bird species richness (5) than Normal Dense buildings (0.83). We ran an ordi- nary least squares model with species richness as the dependent variable, building type, the nearby bird species richness and an interaction term between them as explanatory variables. The significant interaction term shows that the number of species on Dense and Green buildings is lower than nearby populations (small buildings, vegetation and other urban areas). This suggests that for this case study Dense and Green buildings may act as stepping-stones within a wider vegetation net- work, but alone may be too small to provide core habitat for birds. Key words: urban biodiversity, Dense and Green, skyrise greenery, bird Introduction developing green spaces throughout a city to create a network Native vegetation around urban areas is often reduced as cities of urban greenery. One taxa in particular that can benefit from grow in size and density. This has had a negative impact on lo- an enhanced urban greenery network is Avifauna, as they can cal and transient animal populations, in particular those that fly over objects that would be hazardous to ground dwelling are less able to adapt to an urbanised environment (Seto, fauna (such as roads). This gives them the ability to use small Guneralp, and Hutyra 2012). Reducing negative impacts on ur- patches of vegetation as stepping-stones in high-density areas. ban nature is important as it can provide refuge for populations A number of studies have been conducted to see how greening of rare or important species; provide connectivity between nat- the urban environment can benefit bird species diversity and ural locations, through corridors and stepping-stones; and help abundance, primarily in temperate locations (Blair 1999; maintain ecosystems and their services including providing hu- Ferna ´ ndez-Juricic and Jokima ¨ ki 2001; Chamberlain et al. 2007). mans with a sense of well-being (Dearborn and Kark 2010). A One example is in the city of Milan, where the relationship way of mitigating negative impacts on these populations is by between different attributes of greenspace and bird species V C The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2| Journal of Urban Ecology, 2018, Vol. 4, No. 1 diversity and abundance has been investigated (Sanesi et al. and climbing plants, including a variety of fruit bearing trees and 2009) and the changes of the Avifauna over the last century is flowering plants (Fig. 1A). Hotel Viu (a nine storey building) has very well known (Fornasari et al. 2015). Sanesi’ results showed balconies covered with vegetation in the form of climbing plants that diversity and abundance of bird species increased with dis- and planter boxesacrosstwo of its fac ¸ades, and a rooftop garden tance from the city centre, vegetation patch size and maturity covering all of the uppermost floor, with some fruit trees and of vegetation. Fornasari’ results highlighted how the aging of flowering plants (Fig. 1B). Hotel Klima (over 20 storeys tall) has one parks and road trees is linked to a long-term trend of biodiver- whole fac ¸ade covered with climbing plants growing through a sity increase over the last hundred years and the colonization wire mesh (Fig. 1C). and increase in several ‘forest’ bird species over the last 20 years Using Milan as a case study, this research aims to investigate (i.e. the recent rapid increase in Great Spotted Woodpecker how buildings with the Dense and Green building typology Picoides major and European Robin Erithacus rubecula populations). (large-scale high-density buildings incorporating extensive veg- Previous work has shown that increased vertical complexity in etated green elements) compare to Normal Dense buildings natural habitats, in terms of structure (number and complexity (large-scale high-density buildings absent of any vegetation), of tree, multiple canopy layers and leaf area index) and plant adding to the sparse literature on biodiversity’s use of this species richness increases abundance and richness of foraging increasingly more commonplace urban greenery type. bird species, as it permits more niche specialization (Bradbury et al. 2005; Culbert et al. 2013; Casas et al. 2016). It would be expected that complexity in structure and species richness of Methods vegetation in vertical greenspace would have a similar effect. Study sites Vertical gardens that support trees and shrubs may have a bet- ter ability to provide vertical complexity and a wider array of We carried out our study in and around three Dense and Green species than simpler structures (such as perchable greenwalls). buildings, and six Normal Dense buildings in Milan, Italy. In this More recently, research has asked what other innovative study, we define the Dense and Green buildings as being large- methods can be used to green the city, to make it more suitable scale (over nine storeys) and having extensive vegetation on the for biodiversity. This includes research on how bird species use building in the form of green walls, skygardens or roofgardens buildings incorporating skyrise greenery in the form of green roofs (at least 25% of all facades and roofs) (Schro ¨ pfer 2016). To our and roof gardens; private gardens or balcony’s incorporating knowledge, the three Dense and Green buildings sampled were greenery on different building floors (skygardens); and green walls, the only one found to meet this criteria in Milan at the time of or green facades (vertical greenery as climbers or in pots) (Tan and the data collection. We define Normal Dense buildings as being Sia 2005). However, there has only been a limited amount of quan- over nine storeys, having walls birds could perch on (i.e. ledges, titative research in this area, and even less comparing bird species non-green balconies, etc.) and being absent of any vegetation. richness and abundance between these green elements and The six Normal Dense buildings were Torre Porta Romana, corresponding un-vegetated elements (Oberndorfer et al. 2007; Torre Breda, Torre Garibaldi, Viale Angelo Filippetti 29, Torre Williams, Lundholm, and Scott MacIvor 2014). We found that two Velasca and Torre Solaria. The distribution of the each of the peer reviewed articles on this topic in temperate locations. In buildings surveyed can be seen in Fig. 2. Staffordshire (UK), bird species diversity and abundance was com- pared between 27 green and 27 walls without green (bare), with a 2 Bird survey method minimum size of 10 m (Chiquet, Dover, and Mitchell 2013). The results showed that mean bird abundance on greens walls was Our study used the active-search method over a 25-minute pe- approximately three times higher than that of bare walls. Another riod to survey all birds landing on each building (Berry, study at Chicago’s O’Hare international airport (US) found that dif- Lindenmayer, and Driscoll, 2015; Bibby 2004). We conducted all ference in bird species abundance between three green roofs and surveys during the local bird-breeding season (May/June 2017) two bare roofs (all 1500 m ) was significant for one species only, between 6–9 am and in favourable weather conditions, only and only during one season (Washburn et al. 2016). Specifically, surveying each building once. Two surveyors were responsible an average of 1–2 killdeer birds (Charadrius vociferous)were ob- for identifying birds, one with over 20 years’ experience in iden- served per count on green roofs during the breeding season while tifying bird species in the Milan area. Both surveyors used bin- zero were found on bare roofs. In the same study, the diversity oculars to view the building from different angles between 0 and abundance of birds on the green roofs was also qualitatively and 100 m away from each building. We also recorded the back- determined to be lower than in nearby grassland areas. ground richness of bird species at each of the study sites, during Milan provides an interesting case study on which to study the same active-search period. This included any birds in the how bird species diversity may use vertical greenery in the tem- surrounding area, as observed during the active search or flying perate ecozone, as a number of large urban areas have either been overhead. This was possible due to the relatively low density of recently redeveloped over the past few decades or are planned to birds seen around the buildings. We recorded this information be developed in the near future (e.g. Porta Nuova area and Fiera to account for differences in background populations, which Milano City, respectively) (Dezza 2015; Porta Nuova 2017). These may affect the bird species richness on both building types in projects either plan to or have, constructed large-scale high-den- the study, potentially caused by nearby green spaces or other sity buildings. More recently, some high-density buildings in landscape features. Due to the surrounding building density, in Milan have extensively incorporated green elements, including some situations, it was not possible to see all parts of each one of the most well-known global examples of Dense and Green fac ¸ade; however, this was not systematic to either Dense and buildings, the Bosco Verticale (built in 2014). One of the Bosco Green or Normal Dense buildings. Verticale buildings has 26 floors, the other 18. The two other green During the survey, we also observed bird behaviour qualita- buildings that are currently built in Milan are Hotel VIU Milan tively, to see if birds were using buildings opportunistically (built in 2017) and Hotel Klima (built in 2012). Each unit within (only flying onto them for brief periods while moving through Bosco Verticale has a balcony with medium-sized trees, shrubs their home range), or using them preferentially over other Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan | 3 Figure 1. Pictures of three Dense and Green buildings identified in Milan: (A) Bosco Verticale, (B) Hotel VIU and (C) Hotel Klima. Results We detected 20 bird species during the surveys (154 individuals). The richness of species found at each site and in the nearby area can be found in Fig. 3. The abundance of species spotted at the Dense and Green and Normal Dense buildings can be seen in Table 1. A summary of our model results is shown in Fig. 4. The model interaction term had a P-value <0.05. The model shows an increase in bird species richness on Dense and Green build- ings as bird species richness in the nearby area increases. In contrast, Normal Dense buildings only have a tiny increase as bird species richness in nearby area increases. Furthermore, the model shows that Dense and Green building bird diversity to be between approximately two and five times higher than Normal Dense buildings when the nearby level of bird species richness is the same. Discussion Our study provides a first look at the relationship between Dense and Green buildings and bird species diversity in Milan. The result of our surveys shows that in Milan Dense and Green buildings have a higher mean richness of bird species landing on them (5) than large-scale buildings without vegetation (0.83). Figure 2. Distribution of study sites where we conducted bird surveys. Service This may be due to the greenery providing more areas for Layer Credits: Esri, HERE, DeLorme, MapmyIndia, V C OpenStreetMap contributors, species which have been found to preferentially nest, forage and the GIS user community. (for food and nesting materials) and perch (for singing) on tree shrubs and climbing plants at ground level. This corroborates nearby areas, and to make note of their interaction with differ- previous research in temperate countries conducted by Chiquet, ent parts of the building. Dover, and Mitchell (2013) who found birds to use green walls more than bare walls, but contradicts more recent research con- Data analysis ducted by Washburn et al. (2016) who found that for birds there We modelled bird’s use of different building types using a linear was little difference between how they used green and bare ordinary least squares regression with the bird species richness roofs. at each site as the dependent variable. The explanatory vari- During the survey, the number of species sighted on Dense ables in the model were building type (either Dense and Green and Green buildings was lower than background concentrations or Normal Dense); background bird species richness; and an found in nearby areas (small buildings, vegetation and other interaction term between these two variables. All analyses urban areas). This combined with the significance of the model were conducted using R version 3.4.0 (R Core Team 2017). interaction term supports the view that bird species richness on Visualisations were created using the R package ggplot2 and Dense and Green buildings is dependent on the available pool predicted effects were calculated using the effects package of nearby bird species. This is likely due to there being an insuf- (Fox et al. 2003; Wickham 2009: 2). ficient quantity of greenery on the building to provide core bird Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4| Journal of Urban Ecology, 2018, Vol. 4, No. 1 Common Blackbird and Common Starling, previously bred in open woodlands, gardens and parks in Milan since the begin- ning of the last century (Sevesi 1937). The Common Redstart has been present in these same areas since 1945 (Moltoni 1953). The Hooded Crow is a more recent colonizer with a similar ecol- ogy to the aforementioned species, with an established urban population since the mid-1970s (Londei and Maffioli 1989). We did not find more recent colonizer ‘woodland’ birds breeding in Milan parks and gardens on Dense and Green buildings or in their surroundings during our survey period. Although both the Common House Martin and Italian Sparrow (The Italian sparrow Passer italiae is the endemic, vicar- iant form of the House sparrow Passer domesticus, deriving from hybrid speciation with Spanish sparrow Passer hispaniolensis (Brelsford 2011).) are well known as synantropic species using buildings as nesting sites (Fornasari et al. 2015), we only ob- served them on Dense and Green buildings, possibly due to higher habitat differentiation and better food availability. Interestingly, both species have shown a significant decreasing trend over the last few decades (Rete Rurale Nazionale & LIPU 2014), which has been even stronger for the Milan urban area (Fornasari et al. 2015). During the survey, we also noted that Common Wood Pigeons appeared to spend most of their time on Dense and Green buildings in preference to nearby areas. We found high numbers of two bird species (the Feral Pigeon and Common Swift) that have historically thrived in urban areas in general and in Milan in particular (Moltoni, 1953), at higher quantities on Normal Dense buildings than Dense and Figure 3. Bird species richness in and around high-density green buildings incor- porating extensive vegetation (green walls and balcony’s) and normal buildings Green buildings (Table 1). Feral Pigeons are found widely in ur- (without any vegetation). Horizontal bars indicate the mean and vertical bars in- ban areas, and the Common Swift moves to urban areas during dicate the range of species richness at each building type and their respective the breeding season at the arrival of long-distance spring migra- background populations. tion (which is when the surveys took place) (Muller, Werner, P., and Kelcey 2010). Especially in the part of the city centre habitat, limiting their role to stepping-stones within the wider conserving hundreds of Art Nouveau style ‘liberty’ buildings vegetation network. The connectivity between greenspaces is which were built over a 15-year period during the start of the something found to be important for richness and abundance of 20th century. birds in Milan previously (Sanesi et al. 2009). Furthermore, we The presence of the Eurasian Kestrel on Normal Dense build- observed during the surveys that there was an abundance of ur- ings is likely due to it feeding on the swifts found in abundance ban parks and street trees around the green buildings, which in and around two of the buildings during the surveys (Mikula, may require a shorter distance for birds to access at the ground Hromada, and Tryjanowski 2013). As expected, we often saw level, for a similar benefit. this species on the top of buildings despite it having a popula- The ratio between building bird species richness and back- tion crisis during the 1980s (Nova 2002). This species has been ground bird species richness was not linear across all three the most common raptor species in Milan for a long time and sites. As a percentage of those in the background, more were was formerly dependent on traditional tall buildings such as found on Bosco Verticale and Hotel VIU than Hotel Klima. This church belltowers (Sevesi 1937); while today it is more often may be in part due to no fruiting plants being on the green wall, found in the industrial periphery or on new high-rise office and there being little vegetation extruding from wire mesh buildings. housing it, making it difficult for birds to easily perch on it for long periods. Furthermore, species richness may have been Conclusion higher on Bosco Verticale as the selection of tree species for the building was in-part based on whether they can provide food Our results indicate that bird species are at least using Dense for different types of biodiversity, including birds (Boeri 2016). and Green buildings more opportunistically than Normal Dense Lastly, both Hotel VIU and Hotel Klima had more vertical buildings in Milan. This adds to the previous evidence that this complexity in vegetation, with larger trees either layered over greenery type can provide a role in supporting urban diversity shrubs or climbing plants making it a more attractive habitat in the temperate ecozone. Two of the Dense and Green build- for different foraging bird species. ings studied (Bosco Verticale and Hotel VIU) had a considerably It should be noted that the 11 species we found making use higher species richness than the other (Hotel Klima). This may of some of the surveyed buildings (Table 1) are only a part of the be in part due to them having green balconies with fruiting trees pool of 56 bird species observed in the breeding season within that can provide food and a natural nesting place for many bird the Milan borders by Fornasari et al. (2010). Although, due to the species. However, it should be noted that some cliff-nesting short survey period, it may be possible that more species are us- species (such as Common Swifts) have already become well ing these buildings. Most of these 11 species are also the most adapted to the existing urban landscape in Milan, and would commonly found urban bird species in Milan, and some of benefit from this type of building. Should the redevelopment of them, including the Common Wood Pigeon, Eurasian Blackcap, urban areas in Milan (such as Porta Nuova and Fiera Milano Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan | 5 Table 1. Abundance of species found at Dense and Green and Normal Dense buildings (not including birds found in the background) Building type Building Common name Scientific name Count of species Dense and Green Bosco Verticale Common Blackbird Turdus merula 1 Common Redstart Phoenicurus phoenicurus 1 Common Wood Pigeon Columba palumbus 4 Eurasian Blackcap Sylvia atricapilla 1 Eurasian Kestrel Falco tinnunculus 1 Hooded Crow Corvus cornix 4 Italian Sparrow Passer italiae 5 Hotel Klima Common Wood Pigeon Columba palumbus 2 Eurasian Kestrel Falco tinnunculus 1 Hotel VIU Milan Common House Martin Delichon urbicum 1 Common Redstart Phoenicurus phoenicurus 2 Common Starling Sturnus vulgaris 1 Common Wood Pigeon Columba palumbus 2 Feral Pigeon Columba livia domestica 1 Italian Sparrow Passer italiae 2 Normal Dense Torre Breda Common Swift Apus apus 1 Torre Garibaldi Eurasian Kestrel Falco tinnunculus 1 Torre Solaria Common Wood Pigeon Columba palumbus 1 Viale Angelo Filippetti 29 Common Wood Pigeon Columba palumbus 1 Feral Pigeon Columba livia domestica 1 study, it is not possible to determine whether a network of Dense and Green buildings can provide enough habitat to support local bird species populations without corresponding green spaces on the ground. Further research should be conducted to determine if greenery on Dense and Green buildings can achieve this and im- prove breeding success of birds using these buildings. Acknowledgements We would like to thank Michelle Jiang for contributing on lo- gistical arrangements and supplying photographs and other documentation used in our analysis. Funding The research was conducted by the Future Cities Laboratory at the Singapore-ETH Centre, which was established collabora- tively between ETH Zurich and Singapore’s National Research Foundation (FI 370074016) under its Campus for Research Excellence and Technological Enterprise programme. Conflict of interest statement. None declared. References Berry, L. E., Lindenmayer, D. B., and Driscoll, D. A. (2015) ‘Large Figure 4. Model predicted effect of building type on building bird species rich- Unburnt Areas, Not Small Unburnt Patches, Are Needed to ness, controlling for background bird species richness observed during the sur- veys. Numbers in parentheses indicate the standard error (SE) of the model Conserve Avian Diversity in Fire-Prone Landscapes’, Journal of predicted effect. Only the predicted effect within the range of the data is shown. Applied Ecology, 52: 486–95. The model interaction term had a P-value <0.05. Bibby,C.J.(2004) ‘BirdDiversity Survey Methods’,in W.J.Sutherland, I. Newton, and R. Green (eds) Bird Ecology and Conservation: A City) (Dezza 2015; Porta Nuova 2017) involve building large-scale Handbook of Techniques. Oxford: Oxford University Press, 1–15. buildings, planners should consider augmenting ground level Blair, R. B. (1999) ‘Birds and Butterflies along an Urban Gradient: greenery with vegetation on said buildings to increase the Surrogate Taxa for Assessing Biodiversity?’, Ecological amount of supporting habitat for bird species. The provision of Applications, 9: 164–70. fruiting trees and ensuring that the buildings have diverse plant Boeri, S. 2016. A Vertical Forest.Mantova: Corraini Edizioni. species ‘perchable’ surfaces and a complex vertical structure (in- Bradbury, R. B. et al. (2005) ‘Modelling Relationships Between cluding woody shrubs or trees) would also increase their ability Birds and Vegetation Structure Using Airborne LiDAR Data: A to support bird species. However, based on the results of this Review With Case Studies From Agricultural and Woodland Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6| Journal of Urban Ecology, 2018, Vol. 4, No. 1 small town in Slovakia (Report) (Article; Article/Report). Environments’, International Journal of Avian Science, 147: 443–52. doi: 10.1111/j.1474-919x.2005.00438.x. BirdLife Finland. Brelsford, A. (2011) ‘Hybrid Speciation in Birds: Allopatry More Moltoni, E. (1953) Gli uccelli di MIlano citta `. Important than Ecology?’, Molecular Ecology, 20: 3705–7. Muller, N., Werner, P., and Kelcey, J. G. 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(2013) Bats and ‘FORUM: Do Green Roofs Help Urban Biodiversity swifts as food of the European kestrel (Falco tinnunculus) in a Conservation?’, Journal of Applied Ecology, 51: 1643–9. Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Urban Ecology Oxford University Press

Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan

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Abstract

Our study provides a first look at the relationship between large-scale buildings incorporating vegetation (Dense and Green) and bird species richness in Milan, and is one of the studies conducted so far to assess this relationship globally. We carried out our survey in and around three Dense and Green and six high-density buildings with no vegetation (Normal Dense). Dense and Green buildings had a higher mean bird species richness (5) than Normal Dense buildings (0.83). We ran an ordi- nary least squares model with species richness as the dependent variable, building type, the nearby bird species richness and an interaction term between them as explanatory variables. The significant interaction term shows that the number of species on Dense and Green buildings is lower than nearby populations (small buildings, vegetation and other urban areas). This suggests that for this case study Dense and Green buildings may act as stepping-stones within a wider vegetation net- work, but alone may be too small to provide core habitat for birds. Key words: urban biodiversity, Dense and Green, skyrise greenery, bird Introduction developing green spaces throughout a city to create a network Native vegetation around urban areas is often reduced as cities of urban greenery. One taxa in particular that can benefit from grow in size and density. This has had a negative impact on lo- an enhanced urban greenery network is Avifauna, as they can cal and transient animal populations, in particular those that fly over objects that would be hazardous to ground dwelling are less able to adapt to an urbanised environment (Seto, fauna (such as roads). This gives them the ability to use small Guneralp, and Hutyra 2012). Reducing negative impacts on ur- patches of vegetation as stepping-stones in high-density areas. ban nature is important as it can provide refuge for populations A number of studies have been conducted to see how greening of rare or important species; provide connectivity between nat- the urban environment can benefit bird species diversity and ural locations, through corridors and stepping-stones; and help abundance, primarily in temperate locations (Blair 1999; maintain ecosystems and their services including providing hu- Ferna ´ ndez-Juricic and Jokima ¨ ki 2001; Chamberlain et al. 2007). mans with a sense of well-being (Dearborn and Kark 2010). A One example is in the city of Milan, where the relationship way of mitigating negative impacts on these populations is by between different attributes of greenspace and bird species V C The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2| Journal of Urban Ecology, 2018, Vol. 4, No. 1 diversity and abundance has been investigated (Sanesi et al. and climbing plants, including a variety of fruit bearing trees and 2009) and the changes of the Avifauna over the last century is flowering plants (Fig. 1A). Hotel Viu (a nine storey building) has very well known (Fornasari et al. 2015). Sanesi’ results showed balconies covered with vegetation in the form of climbing plants that diversity and abundance of bird species increased with dis- and planter boxesacrosstwo of its fac ¸ades, and a rooftop garden tance from the city centre, vegetation patch size and maturity covering all of the uppermost floor, with some fruit trees and of vegetation. Fornasari’ results highlighted how the aging of flowering plants (Fig. 1B). Hotel Klima (over 20 storeys tall) has one parks and road trees is linked to a long-term trend of biodiver- whole fac ¸ade covered with climbing plants growing through a sity increase over the last hundred years and the colonization wire mesh (Fig. 1C). and increase in several ‘forest’ bird species over the last 20 years Using Milan as a case study, this research aims to investigate (i.e. the recent rapid increase in Great Spotted Woodpecker how buildings with the Dense and Green building typology Picoides major and European Robin Erithacus rubecula populations). (large-scale high-density buildings incorporating extensive veg- Previous work has shown that increased vertical complexity in etated green elements) compare to Normal Dense buildings natural habitats, in terms of structure (number and complexity (large-scale high-density buildings absent of any vegetation), of tree, multiple canopy layers and leaf area index) and plant adding to the sparse literature on biodiversity’s use of this species richness increases abundance and richness of foraging increasingly more commonplace urban greenery type. bird species, as it permits more niche specialization (Bradbury et al. 2005; Culbert et al. 2013; Casas et al. 2016). It would be expected that complexity in structure and species richness of Methods vegetation in vertical greenspace would have a similar effect. Study sites Vertical gardens that support trees and shrubs may have a bet- ter ability to provide vertical complexity and a wider array of We carried out our study in and around three Dense and Green species than simpler structures (such as perchable greenwalls). buildings, and six Normal Dense buildings in Milan, Italy. In this More recently, research has asked what other innovative study, we define the Dense and Green buildings as being large- methods can be used to green the city, to make it more suitable scale (over nine storeys) and having extensive vegetation on the for biodiversity. This includes research on how bird species use building in the form of green walls, skygardens or roofgardens buildings incorporating skyrise greenery in the form of green roofs (at least 25% of all facades and roofs) (Schro ¨ pfer 2016). To our and roof gardens; private gardens or balcony’s incorporating knowledge, the three Dense and Green buildings sampled were greenery on different building floors (skygardens); and green walls, the only one found to meet this criteria in Milan at the time of or green facades (vertical greenery as climbers or in pots) (Tan and the data collection. We define Normal Dense buildings as being Sia 2005). However, there has only been a limited amount of quan- over nine storeys, having walls birds could perch on (i.e. ledges, titative research in this area, and even less comparing bird species non-green balconies, etc.) and being absent of any vegetation. richness and abundance between these green elements and The six Normal Dense buildings were Torre Porta Romana, corresponding un-vegetated elements (Oberndorfer et al. 2007; Torre Breda, Torre Garibaldi, Viale Angelo Filippetti 29, Torre Williams, Lundholm, and Scott MacIvor 2014). We found that two Velasca and Torre Solaria. The distribution of the each of the peer reviewed articles on this topic in temperate locations. In buildings surveyed can be seen in Fig. 2. Staffordshire (UK), bird species diversity and abundance was com- pared between 27 green and 27 walls without green (bare), with a 2 Bird survey method minimum size of 10 m (Chiquet, Dover, and Mitchell 2013). The results showed that mean bird abundance on greens walls was Our study used the active-search method over a 25-minute pe- approximately three times higher than that of bare walls. Another riod to survey all birds landing on each building (Berry, study at Chicago’s O’Hare international airport (US) found that dif- Lindenmayer, and Driscoll, 2015; Bibby 2004). We conducted all ference in bird species abundance between three green roofs and surveys during the local bird-breeding season (May/June 2017) two bare roofs (all 1500 m ) was significant for one species only, between 6–9 am and in favourable weather conditions, only and only during one season (Washburn et al. 2016). Specifically, surveying each building once. Two surveyors were responsible an average of 1–2 killdeer birds (Charadrius vociferous)were ob- for identifying birds, one with over 20 years’ experience in iden- served per count on green roofs during the breeding season while tifying bird species in the Milan area. Both surveyors used bin- zero were found on bare roofs. In the same study, the diversity oculars to view the building from different angles between 0 and abundance of birds on the green roofs was also qualitatively and 100 m away from each building. We also recorded the back- determined to be lower than in nearby grassland areas. ground richness of bird species at each of the study sites, during Milan provides an interesting case study on which to study the same active-search period. This included any birds in the how bird species diversity may use vertical greenery in the tem- surrounding area, as observed during the active search or flying perate ecozone, as a number of large urban areas have either been overhead. This was possible due to the relatively low density of recently redeveloped over the past few decades or are planned to birds seen around the buildings. We recorded this information be developed in the near future (e.g. Porta Nuova area and Fiera to account for differences in background populations, which Milano City, respectively) (Dezza 2015; Porta Nuova 2017). These may affect the bird species richness on both building types in projects either plan to or have, constructed large-scale high-den- the study, potentially caused by nearby green spaces or other sity buildings. More recently, some high-density buildings in landscape features. Due to the surrounding building density, in Milan have extensively incorporated green elements, including some situations, it was not possible to see all parts of each one of the most well-known global examples of Dense and Green fac ¸ade; however, this was not systematic to either Dense and buildings, the Bosco Verticale (built in 2014). One of the Bosco Green or Normal Dense buildings. Verticale buildings has 26 floors, the other 18. The two other green During the survey, we also observed bird behaviour qualita- buildings that are currently built in Milan are Hotel VIU Milan tively, to see if birds were using buildings opportunistically (built in 2017) and Hotel Klima (built in 2012). Each unit within (only flying onto them for brief periods while moving through Bosco Verticale has a balcony with medium-sized trees, shrubs their home range), or using them preferentially over other Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan | 3 Figure 1. Pictures of three Dense and Green buildings identified in Milan: (A) Bosco Verticale, (B) Hotel VIU and (C) Hotel Klima. Results We detected 20 bird species during the surveys (154 individuals). The richness of species found at each site and in the nearby area can be found in Fig. 3. The abundance of species spotted at the Dense and Green and Normal Dense buildings can be seen in Table 1. A summary of our model results is shown in Fig. 4. The model interaction term had a P-value <0.05. The model shows an increase in bird species richness on Dense and Green build- ings as bird species richness in the nearby area increases. In contrast, Normal Dense buildings only have a tiny increase as bird species richness in nearby area increases. Furthermore, the model shows that Dense and Green building bird diversity to be between approximately two and five times higher than Normal Dense buildings when the nearby level of bird species richness is the same. Discussion Our study provides a first look at the relationship between Dense and Green buildings and bird species diversity in Milan. The result of our surveys shows that in Milan Dense and Green buildings have a higher mean richness of bird species landing on them (5) than large-scale buildings without vegetation (0.83). Figure 2. Distribution of study sites where we conducted bird surveys. Service This may be due to the greenery providing more areas for Layer Credits: Esri, HERE, DeLorme, MapmyIndia, V C OpenStreetMap contributors, species which have been found to preferentially nest, forage and the GIS user community. (for food and nesting materials) and perch (for singing) on tree shrubs and climbing plants at ground level. This corroborates nearby areas, and to make note of their interaction with differ- previous research in temperate countries conducted by Chiquet, ent parts of the building. Dover, and Mitchell (2013) who found birds to use green walls more than bare walls, but contradicts more recent research con- Data analysis ducted by Washburn et al. (2016) who found that for birds there We modelled bird’s use of different building types using a linear was little difference between how they used green and bare ordinary least squares regression with the bird species richness roofs. at each site as the dependent variable. The explanatory vari- During the survey, the number of species sighted on Dense ables in the model were building type (either Dense and Green and Green buildings was lower than background concentrations or Normal Dense); background bird species richness; and an found in nearby areas (small buildings, vegetation and other interaction term between these two variables. All analyses urban areas). This combined with the significance of the model were conducted using R version 3.4.0 (R Core Team 2017). interaction term supports the view that bird species richness on Visualisations were created using the R package ggplot2 and Dense and Green buildings is dependent on the available pool predicted effects were calculated using the effects package of nearby bird species. This is likely due to there being an insuf- (Fox et al. 2003; Wickham 2009: 2). ficient quantity of greenery on the building to provide core bird Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4| Journal of Urban Ecology, 2018, Vol. 4, No. 1 Common Blackbird and Common Starling, previously bred in open woodlands, gardens and parks in Milan since the begin- ning of the last century (Sevesi 1937). The Common Redstart has been present in these same areas since 1945 (Moltoni 1953). The Hooded Crow is a more recent colonizer with a similar ecol- ogy to the aforementioned species, with an established urban population since the mid-1970s (Londei and Maffioli 1989). We did not find more recent colonizer ‘woodland’ birds breeding in Milan parks and gardens on Dense and Green buildings or in their surroundings during our survey period. Although both the Common House Martin and Italian Sparrow (The Italian sparrow Passer italiae is the endemic, vicar- iant form of the House sparrow Passer domesticus, deriving from hybrid speciation with Spanish sparrow Passer hispaniolensis (Brelsford 2011).) are well known as synantropic species using buildings as nesting sites (Fornasari et al. 2015), we only ob- served them on Dense and Green buildings, possibly due to higher habitat differentiation and better food availability. Interestingly, both species have shown a significant decreasing trend over the last few decades (Rete Rurale Nazionale & LIPU 2014), which has been even stronger for the Milan urban area (Fornasari et al. 2015). During the survey, we also noted that Common Wood Pigeons appeared to spend most of their time on Dense and Green buildings in preference to nearby areas. We found high numbers of two bird species (the Feral Pigeon and Common Swift) that have historically thrived in urban areas in general and in Milan in particular (Moltoni, 1953), at higher quantities on Normal Dense buildings than Dense and Figure 3. Bird species richness in and around high-density green buildings incor- porating extensive vegetation (green walls and balcony’s) and normal buildings Green buildings (Table 1). Feral Pigeons are found widely in ur- (without any vegetation). Horizontal bars indicate the mean and vertical bars in- ban areas, and the Common Swift moves to urban areas during dicate the range of species richness at each building type and their respective the breeding season at the arrival of long-distance spring migra- background populations. tion (which is when the surveys took place) (Muller, Werner, P., and Kelcey 2010). Especially in the part of the city centre habitat, limiting their role to stepping-stones within the wider conserving hundreds of Art Nouveau style ‘liberty’ buildings vegetation network. The connectivity between greenspaces is which were built over a 15-year period during the start of the something found to be important for richness and abundance of 20th century. birds in Milan previously (Sanesi et al. 2009). Furthermore, we The presence of the Eurasian Kestrel on Normal Dense build- observed during the surveys that there was an abundance of ur- ings is likely due to it feeding on the swifts found in abundance ban parks and street trees around the green buildings, which in and around two of the buildings during the surveys (Mikula, may require a shorter distance for birds to access at the ground Hromada, and Tryjanowski 2013). As expected, we often saw level, for a similar benefit. this species on the top of buildings despite it having a popula- The ratio between building bird species richness and back- tion crisis during the 1980s (Nova 2002). This species has been ground bird species richness was not linear across all three the most common raptor species in Milan for a long time and sites. As a percentage of those in the background, more were was formerly dependent on traditional tall buildings such as found on Bosco Verticale and Hotel VIU than Hotel Klima. This church belltowers (Sevesi 1937); while today it is more often may be in part due to no fruiting plants being on the green wall, found in the industrial periphery or on new high-rise office and there being little vegetation extruding from wire mesh buildings. housing it, making it difficult for birds to easily perch on it for long periods. Furthermore, species richness may have been Conclusion higher on Bosco Verticale as the selection of tree species for the building was in-part based on whether they can provide food Our results indicate that bird species are at least using Dense for different types of biodiversity, including birds (Boeri 2016). and Green buildings more opportunistically than Normal Dense Lastly, both Hotel VIU and Hotel Klima had more vertical buildings in Milan. This adds to the previous evidence that this complexity in vegetation, with larger trees either layered over greenery type can provide a role in supporting urban diversity shrubs or climbing plants making it a more attractive habitat in the temperate ecozone. Two of the Dense and Green build- for different foraging bird species. ings studied (Bosco Verticale and Hotel VIU) had a considerably It should be noted that the 11 species we found making use higher species richness than the other (Hotel Klima). This may of some of the surveyed buildings (Table 1) are only a part of the be in part due to them having green balconies with fruiting trees pool of 56 bird species observed in the breeding season within that can provide food and a natural nesting place for many bird the Milan borders by Fornasari et al. (2010). Although, due to the species. However, it should be noted that some cliff-nesting short survey period, it may be possible that more species are us- species (such as Common Swifts) have already become well ing these buildings. Most of these 11 species are also the most adapted to the existing urban landscape in Milan, and would commonly found urban bird species in Milan, and some of benefit from this type of building. Should the redevelopment of them, including the Common Wood Pigeon, Eurasian Blackcap, urban areas in Milan (such as Porta Nuova and Fiera Milano Downloaded from https://academic.oup.com/jue/article-abstract/4/1/juy001/4924782 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Birds use of vegetated and non-vegetated high-density buildings—a case study of Milan | 5 Table 1. Abundance of species found at Dense and Green and Normal Dense buildings (not including birds found in the background) Building type Building Common name Scientific name Count of species Dense and Green Bosco Verticale Common Blackbird Turdus merula 1 Common Redstart Phoenicurus phoenicurus 1 Common Wood Pigeon Columba palumbus 4 Eurasian Blackcap Sylvia atricapilla 1 Eurasian Kestrel Falco tinnunculus 1 Hooded Crow Corvus cornix 4 Italian Sparrow Passer italiae 5 Hotel Klima Common Wood Pigeon Columba palumbus 2 Eurasian Kestrel Falco tinnunculus 1 Hotel VIU Milan Common House Martin Delichon urbicum 1 Common Redstart Phoenicurus phoenicurus 2 Common Starling Sturnus vulgaris 1 Common Wood Pigeon Columba palumbus 2 Feral Pigeon Columba livia domestica 1 Italian Sparrow Passer italiae 2 Normal Dense Torre Breda Common Swift Apus apus 1 Torre Garibaldi Eurasian Kestrel Falco tinnunculus 1 Torre Solaria Common Wood Pigeon Columba palumbus 1 Viale Angelo Filippetti 29 Common Wood Pigeon Columba palumbus 1 Feral Pigeon Columba livia domestica 1 study, it is not possible to determine whether a network of Dense and Green buildings can provide enough habitat to support local bird species populations without corresponding green spaces on the ground. Further research should be conducted to determine if greenery on Dense and Green buildings can achieve this and im- prove breeding success of birds using these buildings. Acknowledgements We would like to thank Michelle Jiang for contributing on lo- gistical arrangements and supplying photographs and other documentation used in our analysis. Funding The research was conducted by the Future Cities Laboratory at the Singapore-ETH Centre, which was established collabora- tively between ETH Zurich and Singapore’s National Research Foundation (FI 370074016) under its Campus for Research Excellence and Technological Enterprise programme. Conflict of interest statement. None declared. References Berry, L. E., Lindenmayer, D. B., and Driscoll, D. A. (2015) ‘Large Figure 4. Model predicted effect of building type on building bird species rich- Unburnt Areas, Not Small Unburnt Patches, Are Needed to ness, controlling for background bird species richness observed during the sur- veys. 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