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Understanding how built urban form influences biodiversity
Urban Forestry & Urban Greening 13 (2014) 221–226
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Urban Forestry & Urban Greening journal homepage: www.elsevier.com/locate/ufug
Understanding how built urban form influences biodiversity Erik Andersson a,b,∗ , Johan Colding a,b a b
Stockholm Resilience Centre, Stockholm University, Kräftriket 2B, SE-114 19 Stockholm, Sweden The Beijer Institute of Ecological Economics, The Royal Swedish Academy of Sciences, Box 50005, SE-104 05 Stockholm, Sweden
a r t i c l e Keywords: Bird diversity Interspersion Urban ecology Urban form
i n f o
a b s t r a c t This study seeks to contribute to a more complete understanding of how urban form influences biodiversity by investigating the effects of green area distribution and that of built form. We investigated breeding bird diversity in three types of housing development with approximately the same amount of tree cover. No significant differences in terms of bird communities were found between housing types in any of the survey periods. However, detached housing, especially with interspersed trees, had more neotropical insectivores and higher overall diversity of insectivores. Based on our results and theory we suggest a complementary approach to managing biodiversity in urban landscapes – instead of maximising the value and quality of individual patches efforts could go into enhancing over-all landscape quality at the neighbourhood scale by splitting up part of the green infrastructure. The relatively small differences in bird communities also suggest that different stakeholder groups may be engaged in management. © 2013 Elsevier GmbH. All rights reserved.
Introduction Within the coming two decades, the world will see the addition of nearly 1 million km2 of urban areas (McDonald, 2008). Urban development has already generated some of the greatest local extinction rates of species (McKinney, 2002), and is predicted to have the single largest effect on terrestrial ecosystems in the 21st century (Sala et al., 2000). This means that the form and pattern of new urban areas will affect the world’s ecosystems in profound ways. However, knowledge on what role urban form plays in terms of biodiversity is still in its infancy, constituting a black box in urban design and planning. Cities represent self-organising systems of unusual complexity (Portugali, 2000; Batty, 2005; Miller and Page, 2007), comprising different kinds of self-organising systems, such as social networks, economic markets and ecological systems that all interact with each other. Cities without urban planning and design do not lack order, but rather present both highly developed structures and predictable processes, albeit not necessarily the structures and processes that make them well posed to deal with the pressing problems of climate change and loss of biodiversity and ecosystem services (Marcus and Colding, 2011). The professional practice of urban design is geared at trying to influence different selforganising systems in the city, for example pedestrian movement or the distribution of retail, by the structuring and shaping of
∗ Corresponding author at: Stockholm Resilience Centre, Stockholm University, Kräftriket 2B, SE-114 19 Stockholm, Sweden. Tel.: +46 70 191 71 85. E-mail address: [email protected] (E. Andersson). 1618-8667/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ufug.2013.11.002
urban space (e.g. Hillier and Hanson, 1984). Characteristic for urban design is that this is accomplished using very concrete media such as the structuring and shaping of buildings and landscapes, that is, the built form. Hence, urban space as structured and shaped by built form, is used in urban design to intervene in different urban systems, and therefore also the medium that urban designers need to master to shape and navigate urban development in more sustainable directions (Marcus and Colding, 2011). This study seeks to contribute to a more complete understanding of how urban built form influences biodiversity. It is placed in the context of suburban landscapes, which are known to provide diverse mosaics and resources for biodiversity (e.g. Marzluff and Rodewald, 2008). However, the paucity of empirical studies directly comparing spatial organisation of urban development and combinations of land uses/land cover – at this level of urbanisation – has so far generated limited clues for urban design. Nevertheless, a number of ecological studies have addressed how different types of land use influence biodiversity (Fernandez-Juricic, 2000; Smith et al., 2006; Andersson et al., 2007; Colding and Folke, 2009). Moreover, Colding (2007) outlines how different land uses can be configured and combined for greater support of biodiversity and ecosystem services by way of ‘ecological land-use complementation’. Shifting focus from individual areas to whole landscapes potentially opens up new opportunities for design. Within landscape ecology terms like interspersion and juxtaposition have long been used to describe the spatial configuration of different patches in a landscape (e.g. Forman, 1995). Smaller size and higher shape complexity increase the length of borders among different kinds of patches and thus resource accessibility and potential for complementation. Together, complementation and interspersion could
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E. Andersson, J. Colding / Urban Forestry & Urban Greening 13 (2014) 221–226
at least 40 years old. All sites can arguably be called suburban, based both on location (Fig. 1) and general character (Fig. 2). Bird surveys
Fig. 1. Location of field sites in Stockholm. The three site types are apartment buildings, detached houses with interspersed clumps of trees and detached houses adjacent to a larger forest. The smaller map in the lower left corner shows Stockholm’s location within Sweden.
be an interesting tool for finding and promoting synergies when planning and designing new urban development. In this paper we address how urban form influences biodiversity by conducting replicated surveys in Stockholm, Sweden, of avian biodiversity in three types of housing development with approximately the same amount of formally recognised green areas, in this case mixed forest. We analyse and discuss biodiversity differences in terms of species diversity, species composition and functional redundancy. We place our results in the context of urban land use planning at a neighbourhood (sensu Hersperger, 2006) scale and public engagement in green area management. Methods Study area Stockholm is situated at the boundary between the northern hemisphere boreal zone and the mid-European nemoral zone, and at the outlet of the freshwater lake Mälaren into the brackish Baltic Sea (59◦ 20 N, 18◦ 05 E) (Fig. 1). The physical landscape is shaped by the last glacial period 10,000 years ago, followed by human settlement and cultural practices and it consists of fissured bedrock, clay-covered valleys, and a small-scale rough terrain with a range of habitats conveying a relatively high biodiversity. The Stockholm Metropolitan Area hosts a current population of 1.4 million people; it is the most rapidly growing and most densely populated region in Sweden with 2700 inhabitants/km2 (SCB, 2010). Densification has been identified as the most desirable development trajectory (Regionplanekontoret, 2010; Stadsbyggnadskontoret, 2010). Site attributes Three different types of housing areas were investigated: detached houses with interspersed clumps of trees/small groves, detached houses next to a larger woodland (>10 ha), and apartment buildings with extensive treed commons (Fig. 2). All three types are relatively “greener” than many more recent housing developments. Four sites from each category were chosen for the study and subsequently surveyed for breeding birds. All sites had approximately the same amount of non-garden green areas, primarily woodland or treed commons within a sample area of 300 m × 300 m. Sample areas had to be limited to 300 m × 300 m to avoid too much variation within the sampling. Housing areas in Stockholm are limited in size and on a larger scale land use is quite heterogeneous. Average coverage of impervious surfaces was 35%, with no significant differences between the different types of housing. Most of the development took place between 1900 and 1950, and all sites were
We used the point count method of surveying bird species and their abundances at each site (Bibby et al., 2000). Four survey points were located within each site, distanced 100 m apart and at least 100 m from the sample area boundaries. In the areas with housing next to woodlots two of the survey points were located in the woodlot and two in the housing area. Surveys were conducted three times: in early April, late April/early May and late May/early June 2011. We chose survey periods to cover the annual peak in singing activity, from the early breeding resident birds to migrant passerines. Daily surveys were begun at first light, at approximately 5:30 am in early April and from 3:30 am late May/early June, and finished at latest 2.5 h later. This period overlapped with the daily peak in bird vocal activity. Surveys were only conducted in mornings with favourable weather conditions, i.e. low winds and no heavy rain. Each point was surveyed for 5 min and the number and identity of all birds seen or heard within 50 m were recorded, with the exception of overflying individuals. This threshold distance was chosen to capture only those birds located within the site, to avoid double counting birds at two survey points, and because it is substantially less than the maximum distance observers are estimated to be able to differentiate the distance to calling birds (i.e. 65 m, see Alldredge et al., 2007). An additional 5 min was spent walking between the points, where all species seen or heard within 50 m from the path was noted (only presence) to get an as complete as possible species list for the different sites. Due to the density of vegetation, most identification was made acoustically, rather than visually. In cases of uncertainty, the most conservative estimate of abundance was used. Statistical analyses Data were first explored by comparing species numbers and numbers of individuals across sites using one-way ANOVAs. Second, differences and/or similarities in community structure between the three types of housing development were described using non-metrical multidimensional scaling ordination (MDS), a method used to represent relative dissimilarities as distance in low-dimensional space (Clarke, 1993). Stress, or goodness of fit, was calculated as described by Kruskal (1964), within Primer and using 25 iterations. Similarity matrices were based on Bray Curtis distances. Statistical relationships between bird communities were then tested with PERMANOVA analyses, packaged in R as “adonis” in the library (vegan). The program gives a partitioning of multivariate variation according to individual factors in any fully balanced multi-way ANOVA design, with tests done by permutations (Anderson, 2005). Further description can be found in McArdle and Anderson (2001) and Anderson (2001), where the method is referred to as “permutational manova”. Data was analysed in two ways: either untransformed, using the relative abundances of different species, or divided into functional groups based on diet and then computed based on the number of species within the different functional groups. Each survey period was analysed separately, meaning we ran 2 different analyses on each survey result. P-Levels were adjusted accordingly. As the dietary groups differed substantially both in terms of the number of species and the number of individuals we tested species number distributions individually for the three groups using one-way ANOVAs, with adjusted P-levels. Resulting differences were then further investigated in terms of presence and abundance of individual species within the groups. All statistical analyses were done in R (version
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Fig. 2. The three types of housing investigated: (a) detached houses with interspersed clumps of trees/small groves, (b) detached houses next to a larger woodland, and (c) apartment buildings with extensive treed commons.
Table 1 Mean number of species and individuals at the study sites. A are detached houses with interspersed clumps of trees/small groves, B detached houses next to a larger woodland, and C apartment buildings with extensive treed commons. P1 = early April, P2 = late April/early May and P3 = late May/early June. Letters M, I and S indicate dietary type, M = mixed, I = insects and S = seeds and fruit. A
B
C
M A
Number of individuals, P1 Number of species, P1 Number of individuals, P2 Number of species, P2 Number of individuals, P3 Number of species, P3
42.25 11.75 47.5 14.25 42 13.75
35.5 10.25 40 12.75 41 13.5
42.25 11.25 49.5 14 37 12.25
39.5 10 43.75 9.25 29.67 8
I B
C
30.25 9 38 8.25 29 7.6
35.5 8.5 40.5 9 32 8.75
S
A 4.75 1.5 7.75 4.25 15 7
B
C
A
B
C
6.5 1.75 6.75 3.5 9.8 6
5.5 1.25 4.75 2 6 2.75
5.25 1.75 4.25 1.5 2 1
2 1 2.75 1.5 2.2 1.4
2.75 1.25 3.25 1 2.25 1.25
Table 2 Differences between bird communities in the different housing types (MANOVA). Differences based on dietary groups were calculated on the number of species in each group. Period 1 = early April, period 2 = late April/early May and period 3 = late May/early June.
Period 1, all species Period 2, all species Period 3, all species Period 1, diet groups Period 2, diet groups Period 3, diet groups *
Df
SumsOfSqs
MeanSqs
F model
R2
Pr (>F)
2 2 2 2 2 2
0.19372 0.20736 0.2136 0.031942 0.035314 0.086982
0.096861 0.103678 0.106798 0.015971 0.017657 0.043491
1.2881 1.5145 1.4016 0.83741 1.671 4.6132
0.22254 0.25181 0.2375 0.15689 0.27078 0.50621
0.22 0.055 0.132 0.585 0.225 0.007*
P-Level significance for each period was estimated at 0.025 by applying a simple Bonferroni correction.
2.15.1), except the MDS visualisations, which were done in the PRIMER 6 software (Clarke and Gorley, 2006). Results During the study we observed a total of 36 bird species, representing 14 families (see Table 1 and Appendix I). No species encountered were included on the Swedish Red List of threatened taxa (Gärdenfors, 2010). No overall differences were found in the numbers of species or individuals in any of the periods (P-values ranging between 0.41 and 0.72). Nor were any significant differences in terms bird communities found between housing types in any of the survey periods (Fig. 3 and Table 2). The communities were dominated by a number of species generally found in all housing types at relatively high abundances. However, as the season progressed we found a difference in the functional composition between the housing types (Table 2). Throughout the period the omnivores were by far the largest group, both in terms of the number of species and the number of individuals.
Further partitioning of data into dietary groups indicated that insectivores displayed the most evident differences, with significant differences between the housing types in the last survey period (Table 3). The number of species unique to one of the housing types (interspersed) or to interspersed/adjacent increased, even if their relative abundance remained low (Table 4). All of these are insectivores and long distance migrants.
Table 3 Differences between the different housing types in period 3 for the three dietary groups. Diet
Df
Sum Sq
Mean Sq
F value
Pr (>F)
Mixed Insects Seeds and fruit
2 2 2
2.667 41.17 0.50
1.333 20.583 0.25
0.842 11.23 1.286
0.462 0.00359* 0.323
* P-Level significance was estimated at 0.017 by applying a simple Bonferroni correction.
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E. Andersson, J. Colding / Urban Forestry & Urban Greening 13 (2014) 221–226
Fig. 3. 2D-MDS plots illustrating the distribution and distance between sites and housing types. P1 = early April, P2 = late April/early May and P3 = late May/early June.
Discussion It is known that avian diversity is promoted by local variables, such as the presence of native tree cover, berry shrubs, ponds, and fresh water sources that also increase the likelihood of attracting sensitive species. Often the green environments closest to where people live and work are not planned for beyond the local scale, and Table 4 Bird species unique to either interspersed housing or interspersed and adjacent. Notably, all are neo-tropical migrants and specialised insectivores. Species
Only found in:
Number of individuals:
Luscinia luscinia Phylloscopus sibilatrix Phoenicurus phoenicurus Phylloscopus trochilus Sylvia borin Sylvia curruca
Interspersed Adjacent Interspersed and adjacent Interspersed and adjacent Interspersed and adjacent Interspersed and adjacent
1 2 11 12 4 4
not included in comprehensive planning of biodiversity (Colding et al., 2006). However, as in all landscapes, different patches are influenced by their context and the way management is carried out in such a context. Blair (1996) showed that domestic gardens contribute to support bird populations in larger natural lands (Melles et al., 2003), such as parks, due to landscape complementation functions (sensu Dunning et al., 1992). This suggests that beyond-local management is important for supporting biodiversity. Hence, these types of landscape complementary functions should be much more widely considered in the design and establishment of new urban areas and also in the management of areas that can be considered hotspots of urban biodiversity. One objective of this study was to provide a more complete understanding of how urban built form influences biodiversity. Results reveal that overall differences in bird communities were small; the only significant effect of urban form on birds was the late season difference in functional composition. Thus, to provide a more comprehensive verdict on differences of building typologies and their role in promoting biodiversity
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in urban settings is far too premature and deserve further studies. However, as outlined below this article does take a first step towards understanding how built form and spatial structures can be used to influence and promote biodiversity, here in the form of avian diversity. Birds are often divided into urban avoiders, suburban adapters or urban exploiters (Blair, 1996) based on their response to increasing intensity of urbanisation. In this context our study took place at an intermediate level of urbanisation where one might expect primarily adapters. Most resident birds can be expected to be suburban adapters (Marzluff and Rodewald, 2008) while neotropical migrants seem less attracted by cities (Friesen et al., 1995). However, we found the areas with detached housing to be sufficiently attractive for at least some neotropical migrants. While the relative abundance of neotropical migrants unique to interspersed development or interspersed/adjacent was low, the result is nevertheless interesting in ecological terms. We did not investigate this relationship further, but it is likely that detached house garden habitats provide a richer insect fauna relative apartment buildings with treed commons. For example, it has been shown that domestic gardens hold a rich flora of plants (Maurer et al., 2000; Thompson et al., 2003). While more evidence is needed to support the notion that there exist a positive correlation between plant diversity and insect diversity, domestic gardens have been found to support surprisingly high numbers of invertebrates, regardless of garden plants being native or alien (Shapiro, 2002). Hence, it is likely that active management by homeowners (i.e. gardening) provide a richer set of habitats utilised by insects, which in turn may have a positive impact in creating forage for insectivore birds (Andersson et al., 2007). It is an established fact in conservation biology that big is better than small when it comes to habitat patches, and we agree – at least if you look at a patch in isolation. However, based on our results and literature we suggest that small patches may suffice to maintain bird diversity in more developed areas. Evenly distributed, small patches could reduce the average distance to quality habitat in the larger landscape. For example, small clumps of mature trees scattered throughout a residential area could boost biodiversity in gardens and commons. However, with the small scale heterogeneous character of our study area and the spatial scale the birds in the study can be expected to respond to we cannot yet say something more definitive about the complementary potential in interspersion. Nor could we find larger areas of detached housing without either a forest nearby or at least some degree of interspersed trees. Future work should address a fuller range of housing typologies to help us better understand the potential in urban design to promote biodiversity in built up areas. As indicated in our study the effect of more interspersed designs will also depend on the character of the housing area. While this result may suggest that it is better in ecological terms to plan for urban development patterns based on detached housing typologies of interspersed development or interspersed/adjacent rather than apartment buildings with treed commons, the right to access the former areas is limited for a broader set of citizens (i.e. the public). In contrast, designs involving treed commons offer public space for cities that may offer multiple social–ecological benefits in urban development. As our results indicate, public space in areas with apartment buildings may have an ecological baseline not too different from green areas under private ownership and thus hold the same opportunities for improvement (see e.g. Adams, 1994; Cannon et al., 2005; Andersson et al., 2007) as do private gardens.
the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). Thanks also to Mistra (the Foundation for Strategic Environmental Research) for support to the Stockholm Resilience Centre. Two anonymous reviewers provided valuable advice as to the focus of the article.
Acknowledgments
References
This research is part of the Urban Form-project. The authors work has been funded through support and grants received from
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Appendix I. Bird species encountered during surveys in suburban Stockholm, Sweden, with their feeding preferences during spring/summer and migratory status (R = resident, E = Central/southern Europe and N = neo-tropical). Species
Family
Common name
Diet
Migr. Stat.
Anthus trivialis Carduelis carduelis Carduelis chloris
Motacillidae Fringillidae
Tree Pipit Goldfinch
Insects Seeds
N R
Fringillidae Fringillidae Fringillidae
Seeds and fruit Seeds Mixed
R
Carduelis spinus Coccothraustes coccothraustes Columba livia Columba palumbus Corvus corone cornix Corvus monedula Dendrocopos major
European Greenfinch Eurasian Siskin Hawfinch
Columbidae Columbidae
Rock Dove Wood pidgeon
Seeds Seeds
R E
Corvidae
Hooded Crow
Mixed
E
Corvidae Picidae
Mixed Insects
R R
Insects
R/E
Muscicapidae
Jackdaw Greater Spotted Woodpecker European Robin Pied Flycatcher
Insects
N
Fringillidae Corvidae
Chaffinch Eurasian Jay
Mixed Mixed
E R
Muscicapidae
Thrush Nightingale White Wagtail Coal Tit Blue Tit Great Tit House Sparrow & Tree Sparrow Common Redstart Wood Warbler
Insects
N
Insects Mixed Mixed Mixed Seeds
N R R R R
Insects
N
Insects
N
Insects
N
Insects
N
Mixed Insects
R R
Insects Insects
R R
Mixed Mixed Mixed
E R E
Mixed
R
Erithacus rubecula Ficedula hypoleuca Fringilla coelebs Garrulus glandarius Luscinia luscinia Motacilla alba Parus ater Parus caeruleus Parus major Passer domesticus & montanus Phoenicurus phoenicurus Phylloscopus sibilatrix Phylloscopus trochilus Phylloscopus trochilus Pica pica Picus viridis
Muscicapidae
Motacillidae Paridae Paridae Paridae Passeridae Muscicapidae Phylloscopidae Phylloscopidae
Regulus regulus Sitta europaea
Regulidae Sittidae
Sturnus vulgaris Sylvia atricapilla Sylvia curruca
Sturnidae Sylvidae Sylvidae
Turdus iliacus Turdus merula Turdus philomenos Turdus pilaris
Turdidae Turdidae Turdidae
Willow Warbler Garden Warbler Magpie Green Woodpecker Goldcrest Eurasian Nuthatch Starling Blackcap Lesser Whitethroat Redwing Blackbird Song Thrush
Turdidae
Fieldfare
Phylloscopidae Corvidae Picidae
R R
Invertebrates E Insects R/N Insects N
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Urban Forestry & Urban Greening journal homepage: www.elsevier.com/locate/ufug
Understanding how built urban form influences biodiversity Erik Andersson a,b,∗ , Johan Colding a,b a b
Stockholm Resilience Centre, Stockholm University, Kräftriket 2B, SE-114 19 Stockholm, Sweden The Beijer Institute of Ecological Economics, The Royal Swedish Academy of Sciences, Box 50005, SE-104 05 Stockholm, Sweden
a r t i c l e Keywords: Bird diversity Interspersion Urban ecology Urban form
i n f o
a b s t r a c t This study seeks to contribute to a more complete understanding of how urban form influences biodiversity by investigating the effects of green area distribution and that of built form. We investigated breeding bird diversity in three types of housing development with approximately the same amount of tree cover. No significant differences in terms of bird communities were found between housing types in any of the survey periods. However, detached housing, especially with interspersed trees, had more neotropical insectivores and higher overall diversity of insectivores. Based on our results and theory we suggest a complementary approach to managing biodiversity in urban landscapes – instead of maximising the value and quality of individual patches efforts could go into enhancing over-all landscape quality at the neighbourhood scale by splitting up part of the green infrastructure. The relatively small differences in bird communities also suggest that different stakeholder groups may be engaged in management. © 2013 Elsevier GmbH. All rights reserved.
Introduction Within the coming two decades, the world will see the addition of nearly 1 million km2 of urban areas (McDonald, 2008). Urban development has already generated some of the greatest local extinction rates of species (McKinney, 2002), and is predicted to have the single largest effect on terrestrial ecosystems in the 21st century (Sala et al., 2000). This means that the form and pattern of new urban areas will affect the world’s ecosystems in profound ways. However, knowledge on what role urban form plays in terms of biodiversity is still in its infancy, constituting a black box in urban design and planning. Cities represent self-organising systems of unusual complexity (Portugali, 2000; Batty, 2005; Miller and Page, 2007), comprising different kinds of self-organising systems, such as social networks, economic markets and ecological systems that all interact with each other. Cities without urban planning and design do not lack order, but rather present both highly developed structures and predictable processes, albeit not necessarily the structures and processes that make them well posed to deal with the pressing problems of climate change and loss of biodiversity and ecosystem services (Marcus and Colding, 2011). The professional practice of urban design is geared at trying to influence different selforganising systems in the city, for example pedestrian movement or the distribution of retail, by the structuring and shaping of
∗ Corresponding author at: Stockholm Resilience Centre, Stockholm University, Kräftriket 2B, SE-114 19 Stockholm, Sweden. Tel.: +46 70 191 71 85. E-mail address: [email protected] (E. Andersson). 1618-8667/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ufug.2013.11.002
urban space (e.g. Hillier and Hanson, 1984). Characteristic for urban design is that this is accomplished using very concrete media such as the structuring and shaping of buildings and landscapes, that is, the built form. Hence, urban space as structured and shaped by built form, is used in urban design to intervene in different urban systems, and therefore also the medium that urban designers need to master to shape and navigate urban development in more sustainable directions (Marcus and Colding, 2011). This study seeks to contribute to a more complete understanding of how urban built form influences biodiversity. It is placed in the context of suburban landscapes, which are known to provide diverse mosaics and resources for biodiversity (e.g. Marzluff and Rodewald, 2008). However, the paucity of empirical studies directly comparing spatial organisation of urban development and combinations of land uses/land cover – at this level of urbanisation – has so far generated limited clues for urban design. Nevertheless, a number of ecological studies have addressed how different types of land use influence biodiversity (Fernandez-Juricic, 2000; Smith et al., 2006; Andersson et al., 2007; Colding and Folke, 2009). Moreover, Colding (2007) outlines how different land uses can be configured and combined for greater support of biodiversity and ecosystem services by way of ‘ecological land-use complementation’. Shifting focus from individual areas to whole landscapes potentially opens up new opportunities for design. Within landscape ecology terms like interspersion and juxtaposition have long been used to describe the spatial configuration of different patches in a landscape (e.g. Forman, 1995). Smaller size and higher shape complexity increase the length of borders among different kinds of patches and thus resource accessibility and potential for complementation. Together, complementation and interspersion could
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at least 40 years old. All sites can arguably be called suburban, based both on location (Fig. 1) and general character (Fig. 2). Bird surveys
Fig. 1. Location of field sites in Stockholm. The three site types are apartment buildings, detached houses with interspersed clumps of trees and detached houses adjacent to a larger forest. The smaller map in the lower left corner shows Stockholm’s location within Sweden.
be an interesting tool for finding and promoting synergies when planning and designing new urban development. In this paper we address how urban form influences biodiversity by conducting replicated surveys in Stockholm, Sweden, of avian biodiversity in three types of housing development with approximately the same amount of formally recognised green areas, in this case mixed forest. We analyse and discuss biodiversity differences in terms of species diversity, species composition and functional redundancy. We place our results in the context of urban land use planning at a neighbourhood (sensu Hersperger, 2006) scale and public engagement in green area management. Methods Study area Stockholm is situated at the boundary between the northern hemisphere boreal zone and the mid-European nemoral zone, and at the outlet of the freshwater lake Mälaren into the brackish Baltic Sea (59◦ 20 N, 18◦ 05 E) (Fig. 1). The physical landscape is shaped by the last glacial period 10,000 years ago, followed by human settlement and cultural practices and it consists of fissured bedrock, clay-covered valleys, and a small-scale rough terrain with a range of habitats conveying a relatively high biodiversity. The Stockholm Metropolitan Area hosts a current population of 1.4 million people; it is the most rapidly growing and most densely populated region in Sweden with 2700 inhabitants/km2 (SCB, 2010). Densification has been identified as the most desirable development trajectory (Regionplanekontoret, 2010; Stadsbyggnadskontoret, 2010). Site attributes Three different types of housing areas were investigated: detached houses with interspersed clumps of trees/small groves, detached houses next to a larger woodland (>10 ha), and apartment buildings with extensive treed commons (Fig. 2). All three types are relatively “greener” than many more recent housing developments. Four sites from each category were chosen for the study and subsequently surveyed for breeding birds. All sites had approximately the same amount of non-garden green areas, primarily woodland or treed commons within a sample area of 300 m × 300 m. Sample areas had to be limited to 300 m × 300 m to avoid too much variation within the sampling. Housing areas in Stockholm are limited in size and on a larger scale land use is quite heterogeneous. Average coverage of impervious surfaces was 35%, with no significant differences between the different types of housing. Most of the development took place between 1900 and 1950, and all sites were
We used the point count method of surveying bird species and their abundances at each site (Bibby et al., 2000). Four survey points were located within each site, distanced 100 m apart and at least 100 m from the sample area boundaries. In the areas with housing next to woodlots two of the survey points were located in the woodlot and two in the housing area. Surveys were conducted three times: in early April, late April/early May and late May/early June 2011. We chose survey periods to cover the annual peak in singing activity, from the early breeding resident birds to migrant passerines. Daily surveys were begun at first light, at approximately 5:30 am in early April and from 3:30 am late May/early June, and finished at latest 2.5 h later. This period overlapped with the daily peak in bird vocal activity. Surveys were only conducted in mornings with favourable weather conditions, i.e. low winds and no heavy rain. Each point was surveyed for 5 min and the number and identity of all birds seen or heard within 50 m were recorded, with the exception of overflying individuals. This threshold distance was chosen to capture only those birds located within the site, to avoid double counting birds at two survey points, and because it is substantially less than the maximum distance observers are estimated to be able to differentiate the distance to calling birds (i.e. 65 m, see Alldredge et al., 2007). An additional 5 min was spent walking between the points, where all species seen or heard within 50 m from the path was noted (only presence) to get an as complete as possible species list for the different sites. Due to the density of vegetation, most identification was made acoustically, rather than visually. In cases of uncertainty, the most conservative estimate of abundance was used. Statistical analyses Data were first explored by comparing species numbers and numbers of individuals across sites using one-way ANOVAs. Second, differences and/or similarities in community structure between the three types of housing development were described using non-metrical multidimensional scaling ordination (MDS), a method used to represent relative dissimilarities as distance in low-dimensional space (Clarke, 1993). Stress, or goodness of fit, was calculated as described by Kruskal (1964), within Primer and using 25 iterations. Similarity matrices were based on Bray Curtis distances. Statistical relationships between bird communities were then tested with PERMANOVA analyses, packaged in R as “adonis” in the library (vegan). The program gives a partitioning of multivariate variation according to individual factors in any fully balanced multi-way ANOVA design, with tests done by permutations (Anderson, 2005). Further description can be found in McArdle and Anderson (2001) and Anderson (2001), where the method is referred to as “permutational manova”. Data was analysed in two ways: either untransformed, using the relative abundances of different species, or divided into functional groups based on diet and then computed based on the number of species within the different functional groups. Each survey period was analysed separately, meaning we ran 2 different analyses on each survey result. P-Levels were adjusted accordingly. As the dietary groups differed substantially both in terms of the number of species and the number of individuals we tested species number distributions individually for the three groups using one-way ANOVAs, with adjusted P-levels. Resulting differences were then further investigated in terms of presence and abundance of individual species within the groups. All statistical analyses were done in R (version
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Fig. 2. The three types of housing investigated: (a) detached houses with interspersed clumps of trees/small groves, (b) detached houses next to a larger woodland, and (c) apartment buildings with extensive treed commons.
Table 1 Mean number of species and individuals at the study sites. A are detached houses with interspersed clumps of trees/small groves, B detached houses next to a larger woodland, and C apartment buildings with extensive treed commons. P1 = early April, P2 = late April/early May and P3 = late May/early June. Letters M, I and S indicate dietary type, M = mixed, I = insects and S = seeds and fruit. A
B
C
M A
Number of individuals, P1 Number of species, P1 Number of individuals, P2 Number of species, P2 Number of individuals, P3 Number of species, P3
42.25 11.75 47.5 14.25 42 13.75
35.5 10.25 40 12.75 41 13.5
42.25 11.25 49.5 14 37 12.25
39.5 10 43.75 9.25 29.67 8
I B
C
30.25 9 38 8.25 29 7.6
35.5 8.5 40.5 9 32 8.75
S
A 4.75 1.5 7.75 4.25 15 7
B
C
A
B
C
6.5 1.75 6.75 3.5 9.8 6
5.5 1.25 4.75 2 6 2.75
5.25 1.75 4.25 1.5 2 1
2 1 2.75 1.5 2.2 1.4
2.75 1.25 3.25 1 2.25 1.25
Table 2 Differences between bird communities in the different housing types (MANOVA). Differences based on dietary groups were calculated on the number of species in each group. Period 1 = early April, period 2 = late April/early May and period 3 = late May/early June.
Period 1, all species Period 2, all species Period 3, all species Period 1, diet groups Period 2, diet groups Period 3, diet groups *
Df
SumsOfSqs
MeanSqs
F model
R2
Pr (>F)
2 2 2 2 2 2
0.19372 0.20736 0.2136 0.031942 0.035314 0.086982
0.096861 0.103678 0.106798 0.015971 0.017657 0.043491
1.2881 1.5145 1.4016 0.83741 1.671 4.6132
0.22254 0.25181 0.2375 0.15689 0.27078 0.50621
0.22 0.055 0.132 0.585 0.225 0.007*
P-Level significance for each period was estimated at 0.025 by applying a simple Bonferroni correction.
2.15.1), except the MDS visualisations, which were done in the PRIMER 6 software (Clarke and Gorley, 2006). Results During the study we observed a total of 36 bird species, representing 14 families (see Table 1 and Appendix I). No species encountered were included on the Swedish Red List of threatened taxa (Gärdenfors, 2010). No overall differences were found in the numbers of species or individuals in any of the periods (P-values ranging between 0.41 and 0.72). Nor were any significant differences in terms bird communities found between housing types in any of the survey periods (Fig. 3 and Table 2). The communities were dominated by a number of species generally found in all housing types at relatively high abundances. However, as the season progressed we found a difference in the functional composition between the housing types (Table 2). Throughout the period the omnivores were by far the largest group, both in terms of the number of species and the number of individuals.
Further partitioning of data into dietary groups indicated that insectivores displayed the most evident differences, with significant differences between the housing types in the last survey period (Table 3). The number of species unique to one of the housing types (interspersed) or to interspersed/adjacent increased, even if their relative abundance remained low (Table 4). All of these are insectivores and long distance migrants.
Table 3 Differences between the different housing types in period 3 for the three dietary groups. Diet
Df
Sum Sq
Mean Sq
F value
Pr (>F)
Mixed Insects Seeds and fruit
2 2 2
2.667 41.17 0.50
1.333 20.583 0.25
0.842 11.23 1.286
0.462 0.00359* 0.323
* P-Level significance was estimated at 0.017 by applying a simple Bonferroni correction.
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Fig. 3. 2D-MDS plots illustrating the distribution and distance between sites and housing types. P1 = early April, P2 = late April/early May and P3 = late May/early June.
Discussion It is known that avian diversity is promoted by local variables, such as the presence of native tree cover, berry shrubs, ponds, and fresh water sources that also increase the likelihood of attracting sensitive species. Often the green environments closest to where people live and work are not planned for beyond the local scale, and Table 4 Bird species unique to either interspersed housing or interspersed and adjacent. Notably, all are neo-tropical migrants and specialised insectivores. Species
Only found in:
Number of individuals:
Luscinia luscinia Phylloscopus sibilatrix Phoenicurus phoenicurus Phylloscopus trochilus Sylvia borin Sylvia curruca
Interspersed Adjacent Interspersed and adjacent Interspersed and adjacent Interspersed and adjacent Interspersed and adjacent
1 2 11 12 4 4
not included in comprehensive planning of biodiversity (Colding et al., 2006). However, as in all landscapes, different patches are influenced by their context and the way management is carried out in such a context. Blair (1996) showed that domestic gardens contribute to support bird populations in larger natural lands (Melles et al., 2003), such as parks, due to landscape complementation functions (sensu Dunning et al., 1992). This suggests that beyond-local management is important for supporting biodiversity. Hence, these types of landscape complementary functions should be much more widely considered in the design and establishment of new urban areas and also in the management of areas that can be considered hotspots of urban biodiversity. One objective of this study was to provide a more complete understanding of how urban built form influences biodiversity. Results reveal that overall differences in bird communities were small; the only significant effect of urban form on birds was the late season difference in functional composition. Thus, to provide a more comprehensive verdict on differences of building typologies and their role in promoting biodiversity
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in urban settings is far too premature and deserve further studies. However, as outlined below this article does take a first step towards understanding how built form and spatial structures can be used to influence and promote biodiversity, here in the form of avian diversity. Birds are often divided into urban avoiders, suburban adapters or urban exploiters (Blair, 1996) based on their response to increasing intensity of urbanisation. In this context our study took place at an intermediate level of urbanisation where one might expect primarily adapters. Most resident birds can be expected to be suburban adapters (Marzluff and Rodewald, 2008) while neotropical migrants seem less attracted by cities (Friesen et al., 1995). However, we found the areas with detached housing to be sufficiently attractive for at least some neotropical migrants. While the relative abundance of neotropical migrants unique to interspersed development or interspersed/adjacent was low, the result is nevertheless interesting in ecological terms. We did not investigate this relationship further, but it is likely that detached house garden habitats provide a richer insect fauna relative apartment buildings with treed commons. For example, it has been shown that domestic gardens hold a rich flora of plants (Maurer et al., 2000; Thompson et al., 2003). While more evidence is needed to support the notion that there exist a positive correlation between plant diversity and insect diversity, domestic gardens have been found to support surprisingly high numbers of invertebrates, regardless of garden plants being native or alien (Shapiro, 2002). Hence, it is likely that active management by homeowners (i.e. gardening) provide a richer set of habitats utilised by insects, which in turn may have a positive impact in creating forage for insectivore birds (Andersson et al., 2007). It is an established fact in conservation biology that big is better than small when it comes to habitat patches, and we agree – at least if you look at a patch in isolation. However, based on our results and literature we suggest that small patches may suffice to maintain bird diversity in more developed areas. Evenly distributed, small patches could reduce the average distance to quality habitat in the larger landscape. For example, small clumps of mature trees scattered throughout a residential area could boost biodiversity in gardens and commons. However, with the small scale heterogeneous character of our study area and the spatial scale the birds in the study can be expected to respond to we cannot yet say something more definitive about the complementary potential in interspersion. Nor could we find larger areas of detached housing without either a forest nearby or at least some degree of interspersed trees. Future work should address a fuller range of housing typologies to help us better understand the potential in urban design to promote biodiversity in built up areas. As indicated in our study the effect of more interspersed designs will also depend on the character of the housing area. While this result may suggest that it is better in ecological terms to plan for urban development patterns based on detached housing typologies of interspersed development or interspersed/adjacent rather than apartment buildings with treed commons, the right to access the former areas is limited for a broader set of citizens (i.e. the public). In contrast, designs involving treed commons offer public space for cities that may offer multiple social–ecological benefits in urban development. As our results indicate, public space in areas with apartment buildings may have an ecological baseline not too different from green areas under private ownership and thus hold the same opportunities for improvement (see e.g. Adams, 1994; Cannon et al., 2005; Andersson et al., 2007) as do private gardens.
the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). Thanks also to Mistra (the Foundation for Strategic Environmental Research) for support to the Stockholm Resilience Centre. Two anonymous reviewers provided valuable advice as to the focus of the article.
Acknowledgments
References
This research is part of the Urban Form-project. The authors work has been funded through support and grants received from
Adams, L.W., 1994. Urban Wildlife Habitats. University of Minnesota Press, Minneapolis, USA.
Appendix I. Bird species encountered during surveys in suburban Stockholm, Sweden, with their feeding preferences during spring/summer and migratory status (R = resident, E = Central/southern Europe and N = neo-tropical). Species
Family
Common name
Diet
Migr. Stat.
Anthus trivialis Carduelis carduelis Carduelis chloris
Motacillidae Fringillidae
Tree Pipit Goldfinch
Insects Seeds
N R
Fringillidae Fringillidae Fringillidae
Seeds and fruit Seeds Mixed
R
Carduelis spinus Coccothraustes coccothraustes Columba livia Columba palumbus Corvus corone cornix Corvus monedula Dendrocopos major
European Greenfinch Eurasian Siskin Hawfinch
Columbidae Columbidae
Rock Dove Wood pidgeon
Seeds Seeds
R E
Corvidae
Hooded Crow
Mixed
E
Corvidae Picidae
Mixed Insects
R R
Insects
R/E
Muscicapidae
Jackdaw Greater Spotted Woodpecker European Robin Pied Flycatcher
Insects
N
Fringillidae Corvidae
Chaffinch Eurasian Jay
Mixed Mixed
E R
Muscicapidae
Thrush Nightingale White Wagtail Coal Tit Blue Tit Great Tit House Sparrow & Tree Sparrow Common Redstart Wood Warbler
Insects
N
Insects Mixed Mixed Mixed Seeds
N R R R R
Insects
N
Insects
N
Insects
N
Insects
N
Mixed Insects
R R
Insects Insects
R R
Mixed Mixed Mixed
E R E
Mixed
R
Erithacus rubecula Ficedula hypoleuca Fringilla coelebs Garrulus glandarius Luscinia luscinia Motacilla alba Parus ater Parus caeruleus Parus major Passer domesticus & montanus Phoenicurus phoenicurus Phylloscopus sibilatrix Phylloscopus trochilus Phylloscopus trochilus Pica pica Picus viridis
Muscicapidae
Motacillidae Paridae Paridae Paridae Passeridae Muscicapidae Phylloscopidae Phylloscopidae
Regulus regulus Sitta europaea
Regulidae Sittidae
Sturnus vulgaris Sylvia atricapilla Sylvia curruca
Sturnidae Sylvidae Sylvidae
Turdus iliacus Turdus merula Turdus philomenos Turdus pilaris
Turdidae Turdidae Turdidae
Willow Warbler Garden Warbler Magpie Green Woodpecker Goldcrest Eurasian Nuthatch Starling Blackcap Lesser Whitethroat Redwing Blackbird Song Thrush
Turdidae
Fieldfare
Phylloscopidae Corvidae Picidae
R R
Invertebrates E Insects R/N Insects N
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