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What determines occurrence of threatened bird species on urban wastelands?
Biological Conservation 153 (2012) 87–96
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What determines occurrence of threatened bird species on urban wastelands? Peter J. Meffert a,⇑, Frank Dziock b a b
Technische Universität Berlin, Institut für Ökologie, Department for Biodiversity Dynamics, Rothenburgstr. 12, D-12165 Berlin, Germany Animal and Applied Ecology, Faculty of Agriculture/Landscape Management, University of Applied Sciences Dresden, Pillnitzer Platz 2, D-01326 Dresden, Germany
a r t i c l e
i n f o
Article history: Received 28 September 2011 Received in revised form 11 April 2012 Accepted 17 April 2012 Available online 29 June 2012 Keywords: Species of European Conservation concern Urbanisation Boosted regression trees
a b s t r a c t Bird species of cultivated landscapes have been declining dramatically for decades. The main cause for this decline is intensified agricultural practice. At the same time, worldwide urbanisation increases and has severe impacts on land use. Urban wastelands, i.e., unused land within urban agglomerations, are known to provide habitat for endangered animals, but to date systematic research on birds is rare. We aim at assessing environmental characteristics of urban wastelands that meet the requirements of rare and declining bird species. In the city of Berlin, Germany, we surveyed birds on 55 wasteland sites dominated by sparse vegetation. Our analysis includes quantitative measurements of residential human density and degree of sealing at different spatial scales, a detailed vegetation mapping, and data on human intrusion. Boosted regression trees were used to model the occurrence of eight bird Species of European Conservation concern (SPEC). Overall we found 12 SPEC species; for eight data were sufficient to built models. Our findings reveal that the occurrence of endangered bird species depends most strongly on area size and vegetation structure and to a lesser extent on the composition of the urban matrix. On-site features accounted for roughly two third of the explained variance and degree of urbanisation in the surroundings for the remaining one third. Intrusion of humans or dogs had no measurable negative effect on species occurrence. As a rule of thumb, plots above 5 ha harbour SPEC species, those above 7 ha are valuable for several sensitive openland bird species. We show that wasteland habitats have potential for nature conservation that should be considered by urban planners and landscape architects. Knowledge about crucial habitat features (few trees and shrubs, sparse vegetation) enables us to create and maintain urban green spaces that enhance protection of rare and declining species. Urban wastelands may not have the potential to fully compensate for changes and population declines outside urban areas, but they may help to offset the loss of biodiversity in the countryside. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Biodiversity is seriously threatened by humans (McNeely et al., 1995) but the underlying mechanisms are manifold and contended (Swanson, 1995). In particular, species of open cultivated landscapes are declining dramatically and are increasingly threatened (Robinson and Sutherland, 2002). This applies in particular for birds, both in Europe (BirdLife International, 2004), and North America (Peterjohn and Sauer, 1999). Main causes for loss of agricultural biodiversity are high levels of nutrient application which cause an increased growth of herba⇑ Corresponding author. Present address: Dostojewskistr. 1a, D-17491 Greifswald, Germany. Tel.: +49 15201749393. E-mail addresses: [email protected] (P.J. Meffert), [email protected] (F. Dziock). 0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2012.04.018
ceous plants (Kruune, 1964; O’Connor and Shrubb, 1986), increased herbicide use, novel crops and sowing times, land drainage and the associated intensification of grassland management (Newton, 2004), and associated decreased heterogeneity at multiple scales (Benton et al., 2003). In birds, among the main causes of population declines are intensified agricultural practice, the abandonment of marginally productive but high nature value farmland, and the changing scale of agricultural operations (Donald et al., 2001; Henle et al., 2008; Herkert, 1991; Stoate et al., 2001). Additionally, natural processes that remove vegetation and diversify landscapes and habitats, such as fire, shifting sand dunes, or floods, are prevented (Alcàntara-Ayala and Goudie, 2010). All this contributes to the general decrease of open habitats and related species. In consequence, the Index for common farmland birds decreased by 49% from 1980 to 2008 (EBCC, 2010). In general, ‘ground birds’ seem to be much more affected by land-use change, compared to ‘tree birds’ for which the
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similar index increased by one percent in the same period (EBCC, 2010). At the same time, worldwide urbanisation is sprawling (United Nations, 2007). Urbanisation can be defined as the process of human settlement that gradually transforms uninhabited areas into lands including some degree of relatively permanent human presence (Marzluff et al., 2001). These transformation processes threaten biodiversity as agricultural practice does (Czech et al., 2000; McKinney, 2002; Nakamura and Short, 2001). Urbanisation affects birds by changing habitats at multiple scales (Haire et al., 2000; Melles et al., 2003; Renfrew and Ribic, 2008), fragmenting habitats (Crooks et al., 2001), and increasing the levels of direct human disturbances (Hockin et al., 1992). However, there are two opposite observations regarding the effect of urbanisation on species composition. On the one hand, urban areas provide a wide range of habitat types (Gilbert, 1989) resulting in high species numbers in both plants (Kowarik, 2008; Kühn et al., 2004) and animals (Angold et al., 2006; Strauss and Biedermann, 2006). On the other hand, the number of endangered bird species decreases from sparsely built-up areas towards urban centres, probably mainly due to habitat loss and degradation (Sorace and Gustin, 2010). As urbanisation increases and global human population is growing rapidly (United Nations, 2008), another contrary tendency can be observed. Mainly in the industrial nations, many cities are shrinking (Oswalt and Rieniets, 2006). Emerging wasteland sites, e.g. unused land such as brownfields, vacant lots, or other open spaces are known to provide valuable habitats for wildlife (Angold et al., 2006; Eyre et al., 2003; Strauss and Biedermann, 2006). They could have the potential to improving living conditions, enhancing biodiversity, and may contribute to species conservation (Fritsche et al., 2007). Although growing, literature on nature conservation issues in urban agglomerations is underrepresented (Miller and Hobbs, 2002).There are only a few studies on endangered openland birds (e.g. Jones and Bock, 2002; Sorace and Gustin, 2010) and on urban wastelands as these are often unaccessible, less attractive to ornithologists, and of a temporary nature, e.g. compared to parks.
We studied rare and declining bird species on urban wastelands to quantify the relative impacts of area size, vegetation, direct human disturbance, and the urban matrix on their occurrence. Endangered open-land birds have been shown to be sensitive to fragmentation (Henle et al., 2004; Herkert, 1994; Vickery et al., 1994). Further, open-land bird species depend on appropriate habitats rather than on the surrounding urban matrix (Haire et al., 2000). Since urban wastelands differ fundamentally from the surrounding urban matrix in which they are embedded, and if endangered species exploit these special properties, their occurrence should depend on the on-site features rather than on characteristics of the urban matrix. Therefore, we hypothesise that (1) bird Species of European Conservation concern (SPEC) require larger areas compared to non-SPEC species and that (2) the occurrence of openland birds of conservation concern is related to on-site features such as area size, vegetation, or human disturbance, rather than to the urban matrix (residential population density and degree of sealing in the surroundings of each study site).
2. Methods 2.1. Study area and site selection The study was conducted in Berlin, Germany (52°300 200 N 13°230 5600 E). The climate is temperate with an annual mean temperature of 9.8 °C and an average precipitation of 582 mm (DWD, 2006). Berlin has 3.4 million inhabitants and an area of 892 km2 (Amt für Statistik Berlin-Brandenburg, 2010). Wastelands were located by scanning aerial photographs (Senate Department for Urban Development, 2005). We selected all large wastelands that were available and chose smaller ones in order to cover the main gradients, namely area size of a site, intensity of human disturbance, and degree of urbanisation. All wastelands had an open character (for mean and range of coverages see Table 1). Former uses of the sites varied, such as switching yard station, industrial plant, or buildings that had been demolished. Sites were spread
Table 1 Predictor variables, range and mean; Prop. = proportion. Variable description
Minimum
Maximum
Mean
Size of the mapped site (ha) Class of human disturbance (see Table 2) Index of presence and consistency of dogs Index of presence and consistency of humans Plant growth within a year (no, low, medium, high) Inhabitants/ha within a 50 m buffer around the site Inhabitants/ha within a 200 m buffer around the site Inhabitants/ha within a 2000 m buffer around the site Prop. of sealed surface within a 50 m buffer around the site Prop. of sealed surface within a 200 m buffer around the site Prop. of sealed surface within a 2000 m buffer around the site Presence/absence of trees around the site Prop. covered by herbage up to 5 cm height Prop. covered by herbage between 5 and 10 cm height Prop. covered by herbage between 10 and 20 cm height Prop. covered by herbage between 20 and 50 cm height Prop. covered by herbage between 50 and 100 cm height Prop. covered by herbage above 100 cm height Prop. covered by shrubs beneath 1 m height Prop. covered by shrubs above 1 m height Prop. covered by trees beneath 4 m height Prop. covered by trees above 4 m height Prop. covered by buildings Prop. covered by moss Prop. covered by sand Prop. covered by stones, tarmac, concrete or ballast Prop. covered by water Prop. covered by other
0.25 0 0 0 0 0 0.11 19.98 8.53 10.96 18.24 0 0.01 0.01 0.01 0 0 0 0 0 0 0 0 0 0.06 0 0 0
25.50 4 0.63 0.63 3 220.61 253.34 189.06 87.73 89.36 62.08 1 0.58 0.32 0.21 0.22 0.07 0.10 0.08 0.11 0.10 0.23 0.16 0.42 0.90 0.74 0.10 0.08
4.42 1.93 0.04 0.06 1.25 56.37 89.56 89.20 49.37 50.31 42.16 0.47 0.14 0.08 0.07 0.06 0.02 0.01 0.01 0.01 0.01 0.01 0.01 0.03 0.38 0.15 0.00 0.00
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over the whole city, but mainly in the eastern part and in the city centre due to historical reasons. Berlin emerged from almost 100 villages, farms and towns, and until now, its urban form is very diverse and not monocentric. After World War II, the western part of the city was an enclave, and thus left over only a few wastelands. After the reunification of the divided parts of the city in 1990, empty spaces emerged in the band of the former intra-urban border. 2.2. Species of European Conservation concern Species were categorised as threatened if they are listed as Species of European Conservation concern (SPEC; BirdLife International, 2004). We used data of all present birds during breeding season, thus including birds that used the site only for foraging but bred elsewhere. 2.3. Bird survey In 2007 we conducted a bird survey by visiting 55 sites four times during the nesting season between end of April, when also late migratory birds have been arrived, and end of July. We inspected each site three times in the morning and once in the late afternoon during the second activity peak (Aschoff, 1966). Due to the open vegetation structure of the surveyed wastelands, detectability of birds was high, and risk of dual counts of the same bird was low. To avoid observer bias, mapping was done by the same, experienced ornithologist by walking slowly across the entire area. Time spend on each site was proportional to its size, hence, the level of effort was approximately the same per area. Surveys were only conducted when weather conditions were good; no rain, no or low wind, and not above 28 °C in the afternoon since birds are less active during this time (Kendeigh, 1969). We mapped all present birds but barn-swallows Hirundo rustica, house martins Delichon urbica, and swifts Apus apus since these were permanently flying and thus hardly relatable to the study site. 2.4. Environmental data Vegetation structure is an important factor that influences presence of bird species. With an application of very fine-scale measurements of vegetational parameters, we aimed at assessing which characteristics of the vegetation are crucial for each species in an urban setting. For each study site, we mapped vegetation and surface structure in eleven categories of vegetation height and five categories of different surface materials, and calculated proportions of each class per site. After excluding the less reliable of highly correlated variables (Pearson correlation > 0.5), 29 predictor variables remained (Table 1). Plant growth within the same year, depending on use, maintenance and type of ground cover, was estimated and placed into one of four categories (no, low, medium, high). In the literature, many different proxies for urbanisation are used (Marzluff et al., 2001). Our measures for the degree of urbanisation are the proportion of sealed (impervious) surface, and residential population density, since these imply many structural features of an urban matrix. Referring to definitions proposed by Marzluff et al. (2001) our gradient ranges from rural/exurban to suburban and urban within the city centre (Table 1) although it is completely inside the administrative borders of the city of Berlin. Data on sealed area and population density was taken from Environmental Atlas from the municipality of Berlin (Senate Department for Urban Development, 2004, 2006). Proportion of sealed area and population density was calculated for three buffer zones around each site (50 m, 200 m, and 2000 m) using ArcMap 9.2.
Table 2 Intensity of disturbance by human intrusion, including close vicinity of the site. Code
Disturbance intensity
Frequency of human intrusion
0 1 2 3 4
No disturbance Low disturbance Medium disturbance Heavy disturbance Very heavy disturbance
Never or very rarely One or two times per week About every second day Daily Several times a day
Direct disturbance by human intrusion probably plays another crucial role in response of birds to the urban environment. Especially in urban parks and other recreational areas, disturbance has been proven to affect birds (e.g. Fernandez-Juricic et al., 2001; van der Zande and Vos, 1984). To include this factor, we counted pedestrians and unleashed dogs on-site, and estimated disturbance intensity of the closer vicinity. Numbers of humans and dogs were listed simultaneously with bird mapping to gain a proxy for direct human disturbance intensity. Since each site was also inspected in the afternoon, this gives a good approximation for different recreational uses. Index of humans and dogs were calculated as mean number of humans per visit and hectare multiplied by the degree of presence, i.e., one to four visits where we were able to detect humans or dogs, respectively. Since some of the smaller sites were not entered by humans, but nonetheless disturbed by humans walking nearby, we additionally categorised intensity of disturbance in five classes estimated by the observer (Table 2). 2.5. Species-habitat models We analysed eight single Species of European Conservation concern (SPEC): starling Sturnus vulgaris, red-backed shrike Lanius excubitor, crested lark Galerida cristata, kestrel Falco tinnunculus, tree sparrow Passer montanus, tawny pipit Anthus pratensis, wheatear (or northern wheatear) Oenanthe oenanthe, and linnet Carduelis cannabina. All these species are declining in Europe (BirdLife International, 2004) mainly due to land-use change, particularly in agriculture (Bauer et al., 2005; Glutz von Blotzheim, 1985; Hole et al., 2002). The remaining four SPEC species were too rare (green woodpecker Picus viridis, skylark Alauda arvensis, and woodlark Lullula arborea) or too frequent (house sparrow Passer domesticus) to be modelled (Table 3). 2.6. Statistical analyses The relation between area size and species number is known to have the shape of a power-function (MacArthur and Wilson, 1963). As densities differ between those species of conservation concern (SPEC) and those not of concern (non-SPEC) but we were interested in the species-area relationship, i.e., differences in the slope of the power function, we standardised species number to one to achieve relative number of species in relation to total species number and afterwards linearised the function by logarithmising both axes. We used t-tests to compare the slopes of the two linear models. Statistical analysis predicting occurrence of single species and relative density of SPEC, respectively, were accomplished using boosted regression trees (BRT; Elith et al., 2008; Friedman, 2001). This statistical classification and regression tool is known to combine several advantages—it can fit complex nonlinear relationships, automatically handles interaction effects between predictors, and shows a high predictive performance (Elith et al., 2008). This method does not deliver p-values, but uses internal validation processes that require a proportion of the data set to be held back. We used 10-fold cross validation for model development and validation,
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Table 3 Species of European Conservation concern (SPEC) found on urban wastelands in Berlin. Occurrence frequency is the proportion of the 55 sites populated.
a b c
Bird species
Scientific name
Occurrence frequency (%)
SPEC category
Population trend in Europe 1980–2005a
Crested lark Green woodpecker House sparrow Kestrel Linnet Red-backed shrike Skylark Starling Tawny pipit Tree sparrow Wheatear Woodlark
Galerida cristata Picus viridis Passer domesticus Falco tinnunculus Carduelis cannabina Lanius collurio Alauda arvensis Sturnus vulgaris Anthus campestris Passer montanus Oenanthe oenanthe Lullula arborea
23.6 3.6 89.1 14.5 21.8 10.9 5.5 78.2 12.7 61.8 32.7 9.1
SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC
Moderate declineb Moderate increase Moderate decline Moderate decline Moderate decline Stable Moderate decline Moderate decline Steep declinec Moderate decline Moderate decline Uncertain
3 2 3 3 2 3 3 3 3 3 3 2
EBCC (2010). 1982–2005. 1990–2005.
with the benefit of still using the full data set to fit the final model. Measure of model performance was cross-validated correlation, proportion of explained deviance, and AUC of the ROC curve (area under curve of the receiver operation characteristic). Within the BRT model, three terms are used to optimise predictive performance: bag fraction, learning rate, and tree complexity. The bag fraction determines the proportion of data to be selected at each step and therefore the model stochasticity. The learning rate is used to shrink the contribution of each tree as it is added to the model. It was set to 0.001. Tree complexity determines the number of nodes in a tree (Friedman, 2001). Tree complexity was set to two, allowing interactions between two predictors to be modelled. Bag fraction was varied in order to maximise model performance. We analysed presence/absence data, thus a Bernoulli (i.e., binomial) distribution. We used library gbm (version 1.6-3, Ridgeway, 2007) implemented in the software R (R Development Core Team, 2009). Predictor variables which did not improve predictive performance were removed using a dropping procedure via the simplify command of the gbm package (Elith et al., 2008). This procedure starts with an initial cross-validated model containing all predictor variables and then assesses the potential to remove predictors using ten-fold cross-validation. It removes the lowest contributing predictor, computes the change in predictive deviance, and compares it to that obtained when using all predictors. It repeats this process and gives a function that is afterwards used to drop as many variables as do not change predictive deviance towards higher values. The plots shown are partial dependence functions that show the effect of a single predictor variable on the response variable after accounting for the average effects of all other variables in the model. Variable selection was conducted excluding those with a Pearson correlation > 0.5. For boosted regression trees this is not necessary since highly correlated predictor variables do not cause numeric aberrations (Friedman and Meulman, 2003), but it improves the interpretability of results.
3.1. Species-area curve Species number did differ, but dependency of species number on area size sensu MacArthur and Wilson (1963) did not differ in shape between threatened and not threatened species (Fig. 1; ttest of linearised slope: p = 0.68). About half of the species were threatened, regardless of area size. 3.2. Single-species models The model performance, indicated by cross-validated AUC, ranged from acceptable (0.76) to excellent (0.97; Table 4). The number of predictor variables left in the final model varied from two to ten. A table with the relative influence of all predictors that remained in each model is given in Appendix A. All of the following results refer to Fig. 2. It shows the modelled responses of each species to the predictor variables. All but the linnet responded to area size. In five of the eight modelled species it was the most important predictor. Tawny pipit
3. Results Overall, we detected 50 bird species comprised of 4226 individuals, including 12 Species of European Conservation concern (Table 3) comprising 2575 individuals. Crested lark, red-backed shrike, skylark, tawny pipit, wheatear, and woodlark were predominantly breeding on the study sites as indicated by territorial behaviour like singing or fighting males or nests found. Linnet and starling used them mainly for foraging. House and tree sparrows bred in houses in the immediate vicinity, if not available on-site. Green woodpecker and kestrel were only found foraging on the study sites.
Fig. 1. Fitted power-function dependencies of species number on area size for threatened species (Species of European Conservation concern (SPEC), solid circles) and not threatened species (non-SPEC, open circles). Coefficients of the power function regression: species number = b area sizez, number in brackets is standard error: SPEC: b = 2.480 (0.218), z = 0.343 (0.044), R2 = 0.539; non-SPEC: b = 4.685 (0.409), z = 0.377 (0.043), R2 = 0.616; all coefficients are highly significant (p < 0.001).
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Table 4 Performances of boosted regression tree models for single species. CV AUC = 10-fold cross-validated area under curve of the receivier operation characteristic (ROC). All predictor variables for each model are shown in the appendix. Model species
Number of trees
Bag fraction
Deviance explained (%)
Training data AUC
AUC
Standard error
Starling Red-backed shrike Crested lark Kestrel Tree sparrow Tawny pipit Wheatear Linnet
2050 4150 4950 6600 2350 7100 2250 2950
0.5 0.5 0.5 0.7 0.8 0.8 0.9 0.5
32 56 56 88 54 94 56 35
0.93 0.98 0.98 1.00 0.95 1.00 0.97 0.90
0.76 0.92 0.80 0.95 0.94 0.97 0.86 0.86
0.08 0.03 0.07 0.04 0.03 0.02 0.04 0.07
and wheatear had the highest demands for area and their models rely most on area size as indicated by the highest relative contributions (percentages in Fig. 2). Residential human density of the surrounding urban matrix had no measurable influence on kestrel, tawny pipit, and wheatear. Starlings showed a similar response at this scale but a negative one at 2000 m. Another four species responded negatively to residential density at different spatial scales. Occurrence probability was higher beneath about 30 inhabitants/ha in linnets. Threshold values between higher and lower occurrence probabilities that can be derived from partial dependance plots ranged from 70 to 90 inhabitants/ha in the other four species. The degree of sealing within 50, 200, and 2000 m contributed to the models of five species. Kestrel and wheatear were mostly found at wastelands with highly sealed vicinities (200 m and 50 m, respectively). Starlings, crested larks, and linnets were reduced in abundance in areas with more than 30–40% sealing within 2000 m. The cover of shrubs and trees explained occurrence of six of the eight species. Starlings and kestrels were more likely to occur on sites with a few trees. Crested larks, tawny pipits, wheatears, and linnets were found on sites with few or no trees and shrubs. At the grass layer, starlings and red-backed shrikes were mostly found at tall (50–100 cm), crested larks at short (<5 cm) vegetation. Tawny pipits occurred most frequently on sites with about ten percent short grass. Linnets were rarely found on high grass. Sites with >50% sand cover were more often occupied by wheatears and linnets. Neither human intrusion nor occurrence of dogs had a measurable effect on any of the species. Estimated disturbance intensity by human intrusion (cf. Table 2) was positively correlated to the presence of crested larks. 4. Discussion Wastelands in an urban setting provide habitat for a variety of bird species with differing habitat preferences and threat status. Twelve Species of European Conservation concern occurred on wastelands. Across the eight modelled species, habitat quality, quantity, and the urban matrix explained their presence. Direct disturbance by humans or dogs had no measurable negative impact. We discuss the single groups of environmental predictors in the following sections. 4.1. Influence of on-site features 4.1.1. Area size The size of a habitat patch is an important determining factor for both species richness (Donnelly and Marzluff, 2006; Tilghman, 1987) and the occurrence of single species (Davis, 2004; Helzer and Jelinski, 1999). While fragmentation has rather small effects on forest birds (Fahrig, 2001; Trzcinski et al., 1999), many open-land birds are strongly affected by fragmentation (Ribic et al., 2009).
That applies in particular to species that inhabit the interior and avoid the edges (Helzer and Jelinski, 1999; Vickery et al., 1994). We did not measure connectivity asthe counterpart of fragmentation because birds are highly mobile organisms. Most of open-land birds we found are migratory, and examples of e.g. wheatears or tawny pipits in separated wastelands within the city centre show that they settle also on isolated habitat fragments. As we did not measure connectivity, we can not exclude an additional effect of separation of habitats from each other. Our results show that the demand for area is not generally higher for threatened bird species that inhabit urban wastelands up to 25 ha size compared to nonthreatened species (Fig. 1): If threatened species would need larger areas compared to nonthreatened species, the slopes of the regression lines would be different, but they are not (after delogarithmizing both axes to obtain linear functions). We had therefore to reject our initial hypothesis that species of conservation concern require larger areas compared to non-SPEC species. These species seem not to be endangered for high space requirements. Possibly, the observed SPEC species are pre-adapted to fragmentation and thus not very sensitive to the urban matrix. Hence, other SPEC species may need habitat patches exceeding our maximum of 25 ha and did therefore not occur on our study sites. Area requirements for grassland birds vary widely. Depending on species and region, calculated minimum areas in North American grasslands range from 5 to 145 ha (Davis, 2004; Helzer and Jelinski, 1999; Herkert, 1994; Walk and Warner, 1999). In some species, area sensitivity differs regionally (Johnson and Igl, 2001). Area requirements of our study species were rarely examined in urban settings. Our results show the highest occurrence probabilities for single species at 3–7 ha. In accordance with our findings, Triplet (1981) estimated the home range of crested larks at 4.6 ha. Minimum area requirements of tawny pipits in agricultural areas are 7 ha (Caplat and Fonderflick, 2009), which is in line with the threshold of 7 ha we found for urban habitats. Caplat and Fonderflick (2009) refer to wheatear and tawny pipit as ‘area-sensitive species’ (sensu Davis, 2004). Our results confirm their finding but also show that comparatively small urban wastelands seem to provide habitat for these species. 4.1.2. Vegetation and structure Vegetational variables influence species richness, abundance, and composition to a large extent (Gavareski, 1976; Melles et al., 2003; White et al., 2005). Previous studies from urban areas show that habitat quality is an essential factor for occurrence of bird species both in woodlands (Croci et al., 2008; Fahrig, 2001; Trzcinski et al., 1999) and grasslands (Haire et al., 2000). However, openland birds differ fundamentally from woodland species regarding habitat quantity, quality and connectivity. Therefore, also underlying mechanisms may differ but have not been studied as extensive as in woodlands.
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Urban matrix
Other
0.84
0.15 0.05
45%
0.25 0.10
0.25 0.10
16 %
10 % 0 1 2 3 4 Disturbance intensity
0.2
0.0 0.2 0.4 0.6 Proportion grass < 5 cm height
0.1
35 %
0.0
0.0 20 60 Proportion sealed within 200 m 0.9
0.76
0.76
0.84
0.84 0.76 0.10 13 %
0.1
0.1
9%
0.00 0.04 0.08 Proportion shrubs < 1m height 0.2
20 40 60 Proportion sealed within 2000 m 0.2
50 150 Inhabitants/ha within 2000 m
0.0 0.9
12 % 50 150 Inhabitants/ha within 2000 m
0.1
0.10
12 %
0.25
0.25
0.25
0.2
5%
24 %
0.00 0.04 Proportion grass 50-100 cm height
0.00 0.04 Proportion grass 50-100 cm height
10 20 Area size (ha)
0.00 0.04 0.08 Proportion trees < 4 m height
14 %
0.0
0.1 Proportion building
0.6
49 %
0
100 200 Inhabitants/ha within 50 m
0.1
0.1 0.0
0
100 200 Inhabitants/ha within 50 m
17 %
0.10
13 %
no yes Trees around the site
8% 0.2 0.6 Proportion sand
0.25
0.0 0.1 Proportion shrubs > 1m height
0.10 20 40 60 Proportion sealed within 2000 m
0.5
8%
0.1
0.5 31 %
0.10
0.10
15 %
0.25
20 60 Proportion sealed within 50 m 0.25
10 20 Area size (ha)
0.0 0.2 0.4 0.6 Proportion grass < 5 cm height
0.1
0.1
9%
0.25
0.0 0.5
0.5
0.0 0.1 0.2 Proportion trees > 4 m height
75 %
0.1
0.0
0.1 10 20 Area size (ha)
25 %
0.0 0.1 Proportion grass > 100 cm height
0.25
10 20 Area size (ha)
0.10
0.3
0.3
0.6
10 % 0.0 0.1 0.2 Proportion trees > 4 m height
100 200 Inhabitants/ha within 200 m
0.10
0.25 0.10
Occurence probability Occurence probability Occurence probability Occurence probability Occurence probability Occurence probability
0
56 %
0
Linnet
Grass cover
15 %
0
Wheatear
10 % 0.2 0.4 0.6 Proportion sealed within 2000 m
23 %
10 20 Area size (ha)
51 % 0
Tawny pipit
100 200 Inhabitants/ha within 200 m
13 %
0
Tree sparrow
10 20 Area size (ha)
13 % 0
Kestrel
0.84
0.15 16 % 0
Crested lark
12 % 0
0.05
0.15 0.05
Occurence probability
Red-backed shrike
10 20 Area size (ha)
Tree and shrub cover
Degree of sealing
0.76
0.84 19 % 0
0.76
0.84 0.76
Occurence probability
Inhabitants
Starling
On-site vegetation
Area size
0.0
Bird species
24 % 0.2 0.6 Proportion sand
Fig. 2. Modelled occurrence probabilities for eight Species of European Conservation concern (SPEC) in relation to predictor variables. Percentages inside each box indicate relative contribution of the variable.
Since our surveyed waste-land sites were all of an open character, the results do not show the habitat requirements in contrast to other groups such as woodland species but give a more detailed picture for open-land birds. If the demands of a species are less
specific, it comes across many wastelands, as the tree sparrow that did not respond to any on-site variables but area size. Across the eight modelled species, vegetation accounted for about one third of the explained variance. Most species responded positively to
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characteristics of early successional stages as few or no trees and shrubs, and a sparse and short grass layer. Short grass as key-habitat feature for endangered bird species is also reported from North America. From 1900 to the 1990s former common birds associated with short grass disappeared or declined there, whereas species associated with mixed and tallgrass habitats increased or held steady (Jones and Bock, 2002). Similar findings affirm the relevance of short and sparse vegetation for the crested lark in Vienna, Austria. A detailed study by Frank and Wichmann (2003) compared abandoned territories of crested larks with settled ones. Abandoned sites had less lawn, less sparse vegetated wastelands and bare soils, but more shrubs and trees, what is in line with our findings for this species. Vegetational structure seems to be crucial for habitat selection of many bird species. This has been shown for the common redstart (Phoenicurus phoenicurus; Martinez et al., 2010). As wheatear and red-backed shrike, the common redstart is a sitand-wait predator and it also declined dramatically (BirdLife International, 2004). In experiments, it favoured sparse vegetation due to higher detectability of prey, even if prey density was much higher in dense vegetation. Common redstarts assess habitat quality by using vegetation structure as a predictor of food availability, as Tye (1992) found for the wheatear. Also many other bird species prefer short vegetation for foraging (Atkinson et al., 2004). In general, decrease of short grass and sparse vegetation might be connected to application of fertilisers, less extensive grazing or mowing, or increased deposition of atmospheric nitrogen. In this respect urban areas may constitute an exception. Though the comparatively slow succession in the investigation area arises partly from sandy and nutrient-poor soils of the Berlin glacial valley, urban agglomerations may suffer less from eutrophication, since fertilisers are not used in agricultural proportions. Additionally, usual removal of topsoils on wastelands for constructions, elimination of contaminants, or pavement, reduces fertility and thus aids species of early successional stages that can grow in poor soil conditions. 4.1.3. Intrusion of humans and dogs In general, there is strong evidence that direct human disturbance by intrusion has negative impacts on bird diversity, density, and reproduction (e.g. Fernandez-Juricic et al., 2001; Flemming et al., 1988; Gutzwiller et al., 1998; Miller et al., 1998; Westmoreland and Best, 1985). Schlesinger et al. (2008) found that influence of disturbance on bird communities in forest remnants was two times higher than that of habitat loss. Many studies have found interspecific variations in the behavioural responses to human disturbance (Blumstein et al., 2005). In our study, disturbance intensity was positively correlated with occurrence of crested larks. This corresponds well with the described behaviour of this species, that is, flight distances of 1–2 m to humans and 1 m to moving cars (Glutz von Blotzheim, 1985). Explanations for this pattern could be artificial food supply, for instance in front of supermarkets, or a lower risk of predation close to humans. Neither disturbance intensity in the closer vicinity nor density and frequency of humans or dogs on-site explained any variation in the other models. Our study species either have short flight distances when approached by a human (tree sparrow, crested lark) and are thus less sensitive, or inhabit sites that were large enough to avoid encounters with humans and dogs (wheatear, tawny pipit). In contradiction to our initial hypothesis we conclude that the threatened species we investigated seem to have been able to cope with human disturbance in urban settings. The intensity of disturbance on wastelands is in general very low compared to other urban structures such as streets or parks.
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Hence, we did not display the whole gradient of disturbance but the range that can be found on wastelands. For this special kind of habitat we found no crucial role of disturbance intensity. Possibly, especially disturbance-sensitive species avoid the whole urban area and never settle on urban wastelands. Moreover, our study focussed on occurrence only, but not on reproductional success that might be influenced from other factors. 4.2. Influence of the urban matrix Our study species differed to a large extent in their response to the urban matrix in the vicinity of the study sites. Association with the degree of urbanisation covered a range from zero to 49 % of the explained variation. 4.2.1. Spatial scales Seven of the eight species modelled responded to the urban matrix at 50 m, 200 m, or multiple scales, whereas the 2000 m scale had the greatest overall influence on species’ occurrence. Also previous findings revealed that multi-level approaches are necessary for understanding response of birds to patchy systems such as urban agglomerations (Clergeau et al., 2006; Hostetler, 2001; Mazerolle and Villard, 1999; Thornton et al., 2011). The responses at different spatial scales may reflect the variation in matrix suitability among species. Habitat specialists such as wheatears (Clavero and Brotons, 2010) respond very little to the urban matrix, whereas habitat generalists as starling or tree sparrow (Clavero and Brotons, 2010) are affected by the matrix. In some cases the 2000 m buffer zones did overlap. This does not matter in a statistical way but may have strengthen some relationships at this spatial scale. 4.2.2. Human population density Three of the eight species modelled were not associated with the urban matrix (kestrel, tawny pipit, and wheatear). The remaining species were rarely found at very high human densities in the closer vicinity (linnet, tree sparrow) or at a broader scale (red-backed shrike, crested lark, starling). These species occurred more frequently in areas with densities below 80 inhabitants/ha, thus, detached houses, exclusive residential areas, or undeveloped land, partly also perimeter block developments and terraced houses (Senate Department for Urban Development, 2006). There are different possible mechanisms causing the described relationships. Overall structural diversity may be related to population density. Further, matrix features could act as criteria for habitat selection even if they do not affect birds’ fitness (Jones, 2001). Eventually, certain types of the urban matrix may cause barrier effects as shown for birds (Hodgson et al., 2007) and bats (Van Heezik et al., 2010). A special case was the starling that was likely to be found at high residential densities at the 200 m scale but avoided densely settled vicinities at the 2000 m scale. These findings possibly indicate a trade-off between advantages, such as artificial food supply, and disadvantages, such as less appropriate habitats for finding arthropods. Availability of nesting sites could also have contributed to this pattern (Hennings and Edge, 2003). 4.2.3. Degree of sealing Surface sealing had a clear influence on some species but it might affect birds indirectly because it is correlated to other land cover types such as green space. Three species that forage on the ground were rarely found at degrees of sealing beyond about 40% at the 2000 m scale. It is possible that they avoid large housing areas that are characterised by on average 38% sealed surfaces
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(Senate Department for Urban Development, 2004). Kestrels and wheatears favoured high degrees of sealing at the 200 m and 50 m scale, respectively. Both species need short vegetation or bare ground for hunting and may be attracted by sealed soils which may indicate openness, for instance parking lots or left over foundations of destructed buildings. Kestrels may also use wastelands more frequently for foraging if other open habitats are rare. 4.3. Urban wastelands Wastelands have been found to provide habitat for various groups of organisms (Angold et al., 2006; Eyre et al., 2003; Öckinger et al., 2009; Strauss and Biedermann, 2006). After Maurer et al. (2000), the most important group for nature conservation purposes within urban agglomerations are species of dry grassland communities, typical for railway areas or urban wastelands in the city. We also found a considerable number of threatened bird species on this type of habitat. The relevance of wastelands for species protection in cities becomes particularly evident if it is compared to other common forms of urban land use. Kübler (2005) explored avifauna of residential areas of Berlin along an urbanisation gradient on overall 106 ha. Out of 12 Species of European Conservation concern (SPEC) we found on wastelands, only three have been found in five types of other urban land uses, namely starlings, house sparrows, and tree sparrows. Kübler (2005) found another three threatened species that depend on woody vegetation, and thus did not occur on sparsely vegetated wastelands. Ten species were found solely on wastelands. This underlines the uniqueness of open wastelands in the range of urban land-use forms. The early successional stages of the surveyed wastelands will vanish by themselves. Thus, a dynamic cycle of spatiotemporal shifts between disturbance in terms of removal of vegetation— e.g. by mowing, grazing, or temporal use—and secondary succession could maintain open spaces and thereby increase biodiversity. These mechanisms have been shown for plants and insects on urban wastelands (Kattwinkel et al., 2009; Kleyer et al., 2007) and should be considered by urban planners (Kattwinkel et al., 2011). More research is needed for the value of urban wastelands in winter. Possibly, they are an important feeding habitat for crested lark and granivorous bird species, as well as for house and tree sparrows, that are known to suffer from lack of appropriate feeding habitats in winter (Bauer et al., 2005; Hole et al., 2002). If we take the densities of birds that breed on the wastelands (unpublished data, Meffert, 2011) and project them for the sum of all Berlin’s wastelands of about 300 ha (Senate Department for Urban Development, 2008), the following picture emerges. Wastelands provide the complete breeding habitat for the very few remaining tawny pipits (100% of estimated Berlin population of four breeding pairs; Otto and Witt, 2002) and for 100% of 115 breeding pairs of wheatears. Considerable proportions of the populations of red-backed shrikes (15% of 250), woodlarks (29 % of 85), crested larks (48% of 180), linnets (50% of 125) and skylarks (8% of 450) bred on wastelands. Of minor quantitative importance for breeding birds are those areas for starling, tree sparrow, and house sparrow. However, they seem to be attractive for foraging for breeding birds, during the post-breeding season, and also in winter. Thus, the potential of urban wastelands for providing habitat for SPEC species is high for some species at a local scale. In a wider spatial context, population numbers are not as high that they could fully compensate for changes and population declines outside urban areas, but they may help to offset the loss of grasslands on the countryside.
Moreover, wastelands could be a contribution to a more integrative approach in nature conservation that does not strictly separate between valuable protected and other areas. In this analysis, we used only survey and not reproduction data. Therefore, we cannot determine whether urban wastelands are valuable in terms of reproduction and survival. But there is initial evidence that breeding success of wheatears on wastelands seems not to be lower compared to natural habitats (Meffert et al., submitted for publication). Increasingly, our cultivated landscape does not provide significant habitat for biota and such land cover is increasing. As long as we are not able to stop this trend, protection of threatened species within urban agglomerations could partly compensate. 4.4. Implications for urban planning and nature conservation—can you imagine a park without trees? Our results show that some endangered open-land bird species inhabit urban wastelands. As unintentionally provided habitats, wastelands differ in various aspects from planned green spaces. Urban planners may use our findings for the design of green spaces to enhance biodiversity and break with our traditional image of urban green consisting of lawn and trees that not only reduces overall biodiversity, but also separates us from nature (Turner et al., 2004). To provide habitat for open-land birds, territories must be large enough. As a rule of thumb, sites above 5 ha harbour some rare bird species, those above 7 ha are especially valuable for threatened open-land bird species. To decrease disturbance levels by humans and dogs, we recommend areas exceeding 10 ha. Carefully planning of trails also can reduce disturbance to the interior or most valuable areas of the habitat. Some species can be helped by providing structures for nesting, such as piles of stones or gabions for the wheatear. With regard to vegetation, we recommend not to dissect the open space by planting trees and high shrubs. Open soils and sparse and short vegetation are of high value. Thus, we recommend to forego high woody vegetation, or at least to concentrate it in certain places on the edge of the area. In the grass layer, spontaneous vegetation should be included and potentially enriched with varied and local seeds. First examples of agricultural-like green areas in Berlin showed both high acceptance by the residents and high biodiversity (Köstler et al., 2006). In addition, predictions of climate development for the region predict less precipitation and desertification (Gerstengarbe et al., 2003). Adaption to these changes regarding the design of green areas could be used for rethinking, e.g. by avoiding woody vegetation that needs watering and including patches with open soils and sparse vegetation. Acknowledgements We thank Leonie K. Fischer and an anonymous referee for improving early drafts of the manuscript, Barbara Clucas for improving the English, and the German Research Foundation (DFG) for funding (Graduate Research Programme on Urban Ecology 780/3). Appendix A Relative contributions of the predictor variables (%) to explain the occurrence of eight bird species by boosted regression tree models. For description of variables see Table 1.
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P.J. Meffert, F. Dziock / Biological Conservation 153 (2012) 87–96 Table 1
Predictor variable
Area size Inhabitants/ha within 50 m Inhabitants/ha within 200 m Inhabitants/ha within 2000 m Proportion sealed within 50 m Proportion sealed within 200 m Proportion sealed within 2000 m Proportion trees < 4 m height Proportion trees > 4 m height Proportion shrub < 1 m height Proportion shrub > 1 m height Proportion grass < 5 cm height Proportion grass 5–10 cm height Proportion grass 50–100 cm height Proportion grass > 100 cm height Proportion moss Trees around the site Proportion sealed Proportion of sand Disturbance intensity Proportion building
Model Crested lark
Kestrel
Linnet
Red-backed shrike
Starling
Tawny pipit
Tree sparrow
Wheatear
13.0 0.0 0.0 5.4 6.1 0.0 12.4 0.0 7.0 9.4 0.0 16.4 6.7 0.0 8.6 5.1 0.0 0.0 0.0 10.0 0.0
13.2 0.0 0.0 0.0 0.0 12.8 0.0 35.0 0.0 0.0 17.6 0.0 0.0 0.0 0.0 0.0 0.0 7.3 0.0 0.0 14.1
0.0 15.3 0.0 0.0 0.0 0.0 30.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0 16.6 0.0 13.0 0.0 24.3 0.0 0.0
15.7 0.0 23.3 16.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 44.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0
19.2 0.0 11.7 12.0 0.0 0.0 9.5 5.0 9.9 0.0 0.0 8.6 0.0 24.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
56.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 14.8 0.0 0.0 25.0 0.0 4.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0
50.6 49.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
75.2 0.0 0.0 0.0 9.0 0.0 0.0 0.0 0.0 0.0 7.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 8.1 0.0 0.0
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What determines occurrence of threatened bird species on urban wastelands? Peter J. Meffert a,⇑, Frank Dziock b a b
Technische Universität Berlin, Institut für Ökologie, Department for Biodiversity Dynamics, Rothenburgstr. 12, D-12165 Berlin, Germany Animal and Applied Ecology, Faculty of Agriculture/Landscape Management, University of Applied Sciences Dresden, Pillnitzer Platz 2, D-01326 Dresden, Germany
a r t i c l e
i n f o
Article history: Received 28 September 2011 Received in revised form 11 April 2012 Accepted 17 April 2012 Available online 29 June 2012 Keywords: Species of European Conservation concern Urbanisation Boosted regression trees
a b s t r a c t Bird species of cultivated landscapes have been declining dramatically for decades. The main cause for this decline is intensified agricultural practice. At the same time, worldwide urbanisation increases and has severe impacts on land use. Urban wastelands, i.e., unused land within urban agglomerations, are known to provide habitat for endangered animals, but to date systematic research on birds is rare. We aim at assessing environmental characteristics of urban wastelands that meet the requirements of rare and declining bird species. In the city of Berlin, Germany, we surveyed birds on 55 wasteland sites dominated by sparse vegetation. Our analysis includes quantitative measurements of residential human density and degree of sealing at different spatial scales, a detailed vegetation mapping, and data on human intrusion. Boosted regression trees were used to model the occurrence of eight bird Species of European Conservation concern (SPEC). Overall we found 12 SPEC species; for eight data were sufficient to built models. Our findings reveal that the occurrence of endangered bird species depends most strongly on area size and vegetation structure and to a lesser extent on the composition of the urban matrix. On-site features accounted for roughly two third of the explained variance and degree of urbanisation in the surroundings for the remaining one third. Intrusion of humans or dogs had no measurable negative effect on species occurrence. As a rule of thumb, plots above 5 ha harbour SPEC species, those above 7 ha are valuable for several sensitive openland bird species. We show that wasteland habitats have potential for nature conservation that should be considered by urban planners and landscape architects. Knowledge about crucial habitat features (few trees and shrubs, sparse vegetation) enables us to create and maintain urban green spaces that enhance protection of rare and declining species. Urban wastelands may not have the potential to fully compensate for changes and population declines outside urban areas, but they may help to offset the loss of biodiversity in the countryside. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Biodiversity is seriously threatened by humans (McNeely et al., 1995) but the underlying mechanisms are manifold and contended (Swanson, 1995). In particular, species of open cultivated landscapes are declining dramatically and are increasingly threatened (Robinson and Sutherland, 2002). This applies in particular for birds, both in Europe (BirdLife International, 2004), and North America (Peterjohn and Sauer, 1999). Main causes for loss of agricultural biodiversity are high levels of nutrient application which cause an increased growth of herba⇑ Corresponding author. Present address: Dostojewskistr. 1a, D-17491 Greifswald, Germany. Tel.: +49 15201749393. E-mail addresses: [email protected] (P.J. Meffert), [email protected] (F. Dziock). 0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2012.04.018
ceous plants (Kruune, 1964; O’Connor and Shrubb, 1986), increased herbicide use, novel crops and sowing times, land drainage and the associated intensification of grassland management (Newton, 2004), and associated decreased heterogeneity at multiple scales (Benton et al., 2003). In birds, among the main causes of population declines are intensified agricultural practice, the abandonment of marginally productive but high nature value farmland, and the changing scale of agricultural operations (Donald et al., 2001; Henle et al., 2008; Herkert, 1991; Stoate et al., 2001). Additionally, natural processes that remove vegetation and diversify landscapes and habitats, such as fire, shifting sand dunes, or floods, are prevented (Alcàntara-Ayala and Goudie, 2010). All this contributes to the general decrease of open habitats and related species. In consequence, the Index for common farmland birds decreased by 49% from 1980 to 2008 (EBCC, 2010). In general, ‘ground birds’ seem to be much more affected by land-use change, compared to ‘tree birds’ for which the
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similar index increased by one percent in the same period (EBCC, 2010). At the same time, worldwide urbanisation is sprawling (United Nations, 2007). Urbanisation can be defined as the process of human settlement that gradually transforms uninhabited areas into lands including some degree of relatively permanent human presence (Marzluff et al., 2001). These transformation processes threaten biodiversity as agricultural practice does (Czech et al., 2000; McKinney, 2002; Nakamura and Short, 2001). Urbanisation affects birds by changing habitats at multiple scales (Haire et al., 2000; Melles et al., 2003; Renfrew and Ribic, 2008), fragmenting habitats (Crooks et al., 2001), and increasing the levels of direct human disturbances (Hockin et al., 1992). However, there are two opposite observations regarding the effect of urbanisation on species composition. On the one hand, urban areas provide a wide range of habitat types (Gilbert, 1989) resulting in high species numbers in both plants (Kowarik, 2008; Kühn et al., 2004) and animals (Angold et al., 2006; Strauss and Biedermann, 2006). On the other hand, the number of endangered bird species decreases from sparsely built-up areas towards urban centres, probably mainly due to habitat loss and degradation (Sorace and Gustin, 2010). As urbanisation increases and global human population is growing rapidly (United Nations, 2008), another contrary tendency can be observed. Mainly in the industrial nations, many cities are shrinking (Oswalt and Rieniets, 2006). Emerging wasteland sites, e.g. unused land such as brownfields, vacant lots, or other open spaces are known to provide valuable habitats for wildlife (Angold et al., 2006; Eyre et al., 2003; Strauss and Biedermann, 2006). They could have the potential to improving living conditions, enhancing biodiversity, and may contribute to species conservation (Fritsche et al., 2007). Although growing, literature on nature conservation issues in urban agglomerations is underrepresented (Miller and Hobbs, 2002).There are only a few studies on endangered openland birds (e.g. Jones and Bock, 2002; Sorace and Gustin, 2010) and on urban wastelands as these are often unaccessible, less attractive to ornithologists, and of a temporary nature, e.g. compared to parks.
We studied rare and declining bird species on urban wastelands to quantify the relative impacts of area size, vegetation, direct human disturbance, and the urban matrix on their occurrence. Endangered open-land birds have been shown to be sensitive to fragmentation (Henle et al., 2004; Herkert, 1994; Vickery et al., 1994). Further, open-land bird species depend on appropriate habitats rather than on the surrounding urban matrix (Haire et al., 2000). Since urban wastelands differ fundamentally from the surrounding urban matrix in which they are embedded, and if endangered species exploit these special properties, their occurrence should depend on the on-site features rather than on characteristics of the urban matrix. Therefore, we hypothesise that (1) bird Species of European Conservation concern (SPEC) require larger areas compared to non-SPEC species and that (2) the occurrence of openland birds of conservation concern is related to on-site features such as area size, vegetation, or human disturbance, rather than to the urban matrix (residential population density and degree of sealing in the surroundings of each study site).
2. Methods 2.1. Study area and site selection The study was conducted in Berlin, Germany (52°300 200 N 13°230 5600 E). The climate is temperate with an annual mean temperature of 9.8 °C and an average precipitation of 582 mm (DWD, 2006). Berlin has 3.4 million inhabitants and an area of 892 km2 (Amt für Statistik Berlin-Brandenburg, 2010). Wastelands were located by scanning aerial photographs (Senate Department for Urban Development, 2005). We selected all large wastelands that were available and chose smaller ones in order to cover the main gradients, namely area size of a site, intensity of human disturbance, and degree of urbanisation. All wastelands had an open character (for mean and range of coverages see Table 1). Former uses of the sites varied, such as switching yard station, industrial plant, or buildings that had been demolished. Sites were spread
Table 1 Predictor variables, range and mean; Prop. = proportion. Variable description
Minimum
Maximum
Mean
Size of the mapped site (ha) Class of human disturbance (see Table 2) Index of presence and consistency of dogs Index of presence and consistency of humans Plant growth within a year (no, low, medium, high) Inhabitants/ha within a 50 m buffer around the site Inhabitants/ha within a 200 m buffer around the site Inhabitants/ha within a 2000 m buffer around the site Prop. of sealed surface within a 50 m buffer around the site Prop. of sealed surface within a 200 m buffer around the site Prop. of sealed surface within a 2000 m buffer around the site Presence/absence of trees around the site Prop. covered by herbage up to 5 cm height Prop. covered by herbage between 5 and 10 cm height Prop. covered by herbage between 10 and 20 cm height Prop. covered by herbage between 20 and 50 cm height Prop. covered by herbage between 50 and 100 cm height Prop. covered by herbage above 100 cm height Prop. covered by shrubs beneath 1 m height Prop. covered by shrubs above 1 m height Prop. covered by trees beneath 4 m height Prop. covered by trees above 4 m height Prop. covered by buildings Prop. covered by moss Prop. covered by sand Prop. covered by stones, tarmac, concrete or ballast Prop. covered by water Prop. covered by other
0.25 0 0 0 0 0 0.11 19.98 8.53 10.96 18.24 0 0.01 0.01 0.01 0 0 0 0 0 0 0 0 0 0.06 0 0 0
25.50 4 0.63 0.63 3 220.61 253.34 189.06 87.73 89.36 62.08 1 0.58 0.32 0.21 0.22 0.07 0.10 0.08 0.11 0.10 0.23 0.16 0.42 0.90 0.74 0.10 0.08
4.42 1.93 0.04 0.06 1.25 56.37 89.56 89.20 49.37 50.31 42.16 0.47 0.14 0.08 0.07 0.06 0.02 0.01 0.01 0.01 0.01 0.01 0.01 0.03 0.38 0.15 0.00 0.00
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over the whole city, but mainly in the eastern part and in the city centre due to historical reasons. Berlin emerged from almost 100 villages, farms and towns, and until now, its urban form is very diverse and not monocentric. After World War II, the western part of the city was an enclave, and thus left over only a few wastelands. After the reunification of the divided parts of the city in 1990, empty spaces emerged in the band of the former intra-urban border. 2.2. Species of European Conservation concern Species were categorised as threatened if they are listed as Species of European Conservation concern (SPEC; BirdLife International, 2004). We used data of all present birds during breeding season, thus including birds that used the site only for foraging but bred elsewhere. 2.3. Bird survey In 2007 we conducted a bird survey by visiting 55 sites four times during the nesting season between end of April, when also late migratory birds have been arrived, and end of July. We inspected each site three times in the morning and once in the late afternoon during the second activity peak (Aschoff, 1966). Due to the open vegetation structure of the surveyed wastelands, detectability of birds was high, and risk of dual counts of the same bird was low. To avoid observer bias, mapping was done by the same, experienced ornithologist by walking slowly across the entire area. Time spend on each site was proportional to its size, hence, the level of effort was approximately the same per area. Surveys were only conducted when weather conditions were good; no rain, no or low wind, and not above 28 °C in the afternoon since birds are less active during this time (Kendeigh, 1969). We mapped all present birds but barn-swallows Hirundo rustica, house martins Delichon urbica, and swifts Apus apus since these were permanently flying and thus hardly relatable to the study site. 2.4. Environmental data Vegetation structure is an important factor that influences presence of bird species. With an application of very fine-scale measurements of vegetational parameters, we aimed at assessing which characteristics of the vegetation are crucial for each species in an urban setting. For each study site, we mapped vegetation and surface structure in eleven categories of vegetation height and five categories of different surface materials, and calculated proportions of each class per site. After excluding the less reliable of highly correlated variables (Pearson correlation > 0.5), 29 predictor variables remained (Table 1). Plant growth within the same year, depending on use, maintenance and type of ground cover, was estimated and placed into one of four categories (no, low, medium, high). In the literature, many different proxies for urbanisation are used (Marzluff et al., 2001). Our measures for the degree of urbanisation are the proportion of sealed (impervious) surface, and residential population density, since these imply many structural features of an urban matrix. Referring to definitions proposed by Marzluff et al. (2001) our gradient ranges from rural/exurban to suburban and urban within the city centre (Table 1) although it is completely inside the administrative borders of the city of Berlin. Data on sealed area and population density was taken from Environmental Atlas from the municipality of Berlin (Senate Department for Urban Development, 2004, 2006). Proportion of sealed area and population density was calculated for three buffer zones around each site (50 m, 200 m, and 2000 m) using ArcMap 9.2.
Table 2 Intensity of disturbance by human intrusion, including close vicinity of the site. Code
Disturbance intensity
Frequency of human intrusion
0 1 2 3 4
No disturbance Low disturbance Medium disturbance Heavy disturbance Very heavy disturbance
Never or very rarely One or two times per week About every second day Daily Several times a day
Direct disturbance by human intrusion probably plays another crucial role in response of birds to the urban environment. Especially in urban parks and other recreational areas, disturbance has been proven to affect birds (e.g. Fernandez-Juricic et al., 2001; van der Zande and Vos, 1984). To include this factor, we counted pedestrians and unleashed dogs on-site, and estimated disturbance intensity of the closer vicinity. Numbers of humans and dogs were listed simultaneously with bird mapping to gain a proxy for direct human disturbance intensity. Since each site was also inspected in the afternoon, this gives a good approximation for different recreational uses. Index of humans and dogs were calculated as mean number of humans per visit and hectare multiplied by the degree of presence, i.e., one to four visits where we were able to detect humans or dogs, respectively. Since some of the smaller sites were not entered by humans, but nonetheless disturbed by humans walking nearby, we additionally categorised intensity of disturbance in five classes estimated by the observer (Table 2). 2.5. Species-habitat models We analysed eight single Species of European Conservation concern (SPEC): starling Sturnus vulgaris, red-backed shrike Lanius excubitor, crested lark Galerida cristata, kestrel Falco tinnunculus, tree sparrow Passer montanus, tawny pipit Anthus pratensis, wheatear (or northern wheatear) Oenanthe oenanthe, and linnet Carduelis cannabina. All these species are declining in Europe (BirdLife International, 2004) mainly due to land-use change, particularly in agriculture (Bauer et al., 2005; Glutz von Blotzheim, 1985; Hole et al., 2002). The remaining four SPEC species were too rare (green woodpecker Picus viridis, skylark Alauda arvensis, and woodlark Lullula arborea) or too frequent (house sparrow Passer domesticus) to be modelled (Table 3). 2.6. Statistical analyses The relation between area size and species number is known to have the shape of a power-function (MacArthur and Wilson, 1963). As densities differ between those species of conservation concern (SPEC) and those not of concern (non-SPEC) but we were interested in the species-area relationship, i.e., differences in the slope of the power function, we standardised species number to one to achieve relative number of species in relation to total species number and afterwards linearised the function by logarithmising both axes. We used t-tests to compare the slopes of the two linear models. Statistical analysis predicting occurrence of single species and relative density of SPEC, respectively, were accomplished using boosted regression trees (BRT; Elith et al., 2008; Friedman, 2001). This statistical classification and regression tool is known to combine several advantages—it can fit complex nonlinear relationships, automatically handles interaction effects between predictors, and shows a high predictive performance (Elith et al., 2008). This method does not deliver p-values, but uses internal validation processes that require a proportion of the data set to be held back. We used 10-fold cross validation for model development and validation,
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Table 3 Species of European Conservation concern (SPEC) found on urban wastelands in Berlin. Occurrence frequency is the proportion of the 55 sites populated.
a b c
Bird species
Scientific name
Occurrence frequency (%)
SPEC category
Population trend in Europe 1980–2005a
Crested lark Green woodpecker House sparrow Kestrel Linnet Red-backed shrike Skylark Starling Tawny pipit Tree sparrow Wheatear Woodlark
Galerida cristata Picus viridis Passer domesticus Falco tinnunculus Carduelis cannabina Lanius collurio Alauda arvensis Sturnus vulgaris Anthus campestris Passer montanus Oenanthe oenanthe Lullula arborea
23.6 3.6 89.1 14.5 21.8 10.9 5.5 78.2 12.7 61.8 32.7 9.1
SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC SPEC
Moderate declineb Moderate increase Moderate decline Moderate decline Moderate decline Stable Moderate decline Moderate decline Steep declinec Moderate decline Moderate decline Uncertain
3 2 3 3 2 3 3 3 3 3 3 2
EBCC (2010). 1982–2005. 1990–2005.
with the benefit of still using the full data set to fit the final model. Measure of model performance was cross-validated correlation, proportion of explained deviance, and AUC of the ROC curve (area under curve of the receiver operation characteristic). Within the BRT model, three terms are used to optimise predictive performance: bag fraction, learning rate, and tree complexity. The bag fraction determines the proportion of data to be selected at each step and therefore the model stochasticity. The learning rate is used to shrink the contribution of each tree as it is added to the model. It was set to 0.001. Tree complexity determines the number of nodes in a tree (Friedman, 2001). Tree complexity was set to two, allowing interactions between two predictors to be modelled. Bag fraction was varied in order to maximise model performance. We analysed presence/absence data, thus a Bernoulli (i.e., binomial) distribution. We used library gbm (version 1.6-3, Ridgeway, 2007) implemented in the software R (R Development Core Team, 2009). Predictor variables which did not improve predictive performance were removed using a dropping procedure via the simplify command of the gbm package (Elith et al., 2008). This procedure starts with an initial cross-validated model containing all predictor variables and then assesses the potential to remove predictors using ten-fold cross-validation. It removes the lowest contributing predictor, computes the change in predictive deviance, and compares it to that obtained when using all predictors. It repeats this process and gives a function that is afterwards used to drop as many variables as do not change predictive deviance towards higher values. The plots shown are partial dependence functions that show the effect of a single predictor variable on the response variable after accounting for the average effects of all other variables in the model. Variable selection was conducted excluding those with a Pearson correlation > 0.5. For boosted regression trees this is not necessary since highly correlated predictor variables do not cause numeric aberrations (Friedman and Meulman, 2003), but it improves the interpretability of results.
3.1. Species-area curve Species number did differ, but dependency of species number on area size sensu MacArthur and Wilson (1963) did not differ in shape between threatened and not threatened species (Fig. 1; ttest of linearised slope: p = 0.68). About half of the species were threatened, regardless of area size. 3.2. Single-species models The model performance, indicated by cross-validated AUC, ranged from acceptable (0.76) to excellent (0.97; Table 4). The number of predictor variables left in the final model varied from two to ten. A table with the relative influence of all predictors that remained in each model is given in Appendix A. All of the following results refer to Fig. 2. It shows the modelled responses of each species to the predictor variables. All but the linnet responded to area size. In five of the eight modelled species it was the most important predictor. Tawny pipit
3. Results Overall, we detected 50 bird species comprised of 4226 individuals, including 12 Species of European Conservation concern (Table 3) comprising 2575 individuals. Crested lark, red-backed shrike, skylark, tawny pipit, wheatear, and woodlark were predominantly breeding on the study sites as indicated by territorial behaviour like singing or fighting males or nests found. Linnet and starling used them mainly for foraging. House and tree sparrows bred in houses in the immediate vicinity, if not available on-site. Green woodpecker and kestrel were only found foraging on the study sites.
Fig. 1. Fitted power-function dependencies of species number on area size for threatened species (Species of European Conservation concern (SPEC), solid circles) and not threatened species (non-SPEC, open circles). Coefficients of the power function regression: species number = b area sizez, number in brackets is standard error: SPEC: b = 2.480 (0.218), z = 0.343 (0.044), R2 = 0.539; non-SPEC: b = 4.685 (0.409), z = 0.377 (0.043), R2 = 0.616; all coefficients are highly significant (p < 0.001).
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Table 4 Performances of boosted regression tree models for single species. CV AUC = 10-fold cross-validated area under curve of the receivier operation characteristic (ROC). All predictor variables for each model are shown in the appendix. Model species
Number of trees
Bag fraction
Deviance explained (%)
Training data AUC
AUC
Standard error
Starling Red-backed shrike Crested lark Kestrel Tree sparrow Tawny pipit Wheatear Linnet
2050 4150 4950 6600 2350 7100 2250 2950
0.5 0.5 0.5 0.7 0.8 0.8 0.9 0.5
32 56 56 88 54 94 56 35
0.93 0.98 0.98 1.00 0.95 1.00 0.97 0.90
0.76 0.92 0.80 0.95 0.94 0.97 0.86 0.86
0.08 0.03 0.07 0.04 0.03 0.02 0.04 0.07
and wheatear had the highest demands for area and their models rely most on area size as indicated by the highest relative contributions (percentages in Fig. 2). Residential human density of the surrounding urban matrix had no measurable influence on kestrel, tawny pipit, and wheatear. Starlings showed a similar response at this scale but a negative one at 2000 m. Another four species responded negatively to residential density at different spatial scales. Occurrence probability was higher beneath about 30 inhabitants/ha in linnets. Threshold values between higher and lower occurrence probabilities that can be derived from partial dependance plots ranged from 70 to 90 inhabitants/ha in the other four species. The degree of sealing within 50, 200, and 2000 m contributed to the models of five species. Kestrel and wheatear were mostly found at wastelands with highly sealed vicinities (200 m and 50 m, respectively). Starlings, crested larks, and linnets were reduced in abundance in areas with more than 30–40% sealing within 2000 m. The cover of shrubs and trees explained occurrence of six of the eight species. Starlings and kestrels were more likely to occur on sites with a few trees. Crested larks, tawny pipits, wheatears, and linnets were found on sites with few or no trees and shrubs. At the grass layer, starlings and red-backed shrikes were mostly found at tall (50–100 cm), crested larks at short (<5 cm) vegetation. Tawny pipits occurred most frequently on sites with about ten percent short grass. Linnets were rarely found on high grass. Sites with >50% sand cover were more often occupied by wheatears and linnets. Neither human intrusion nor occurrence of dogs had a measurable effect on any of the species. Estimated disturbance intensity by human intrusion (cf. Table 2) was positively correlated to the presence of crested larks. 4. Discussion Wastelands in an urban setting provide habitat for a variety of bird species with differing habitat preferences and threat status. Twelve Species of European Conservation concern occurred on wastelands. Across the eight modelled species, habitat quality, quantity, and the urban matrix explained their presence. Direct disturbance by humans or dogs had no measurable negative impact. We discuss the single groups of environmental predictors in the following sections. 4.1. Influence of on-site features 4.1.1. Area size The size of a habitat patch is an important determining factor for both species richness (Donnelly and Marzluff, 2006; Tilghman, 1987) and the occurrence of single species (Davis, 2004; Helzer and Jelinski, 1999). While fragmentation has rather small effects on forest birds (Fahrig, 2001; Trzcinski et al., 1999), many open-land birds are strongly affected by fragmentation (Ribic et al., 2009).
That applies in particular to species that inhabit the interior and avoid the edges (Helzer and Jelinski, 1999; Vickery et al., 1994). We did not measure connectivity asthe counterpart of fragmentation because birds are highly mobile organisms. Most of open-land birds we found are migratory, and examples of e.g. wheatears or tawny pipits in separated wastelands within the city centre show that they settle also on isolated habitat fragments. As we did not measure connectivity, we can not exclude an additional effect of separation of habitats from each other. Our results show that the demand for area is not generally higher for threatened bird species that inhabit urban wastelands up to 25 ha size compared to nonthreatened species (Fig. 1): If threatened species would need larger areas compared to nonthreatened species, the slopes of the regression lines would be different, but they are not (after delogarithmizing both axes to obtain linear functions). We had therefore to reject our initial hypothesis that species of conservation concern require larger areas compared to non-SPEC species. These species seem not to be endangered for high space requirements. Possibly, the observed SPEC species are pre-adapted to fragmentation and thus not very sensitive to the urban matrix. Hence, other SPEC species may need habitat patches exceeding our maximum of 25 ha and did therefore not occur on our study sites. Area requirements for grassland birds vary widely. Depending on species and region, calculated minimum areas in North American grasslands range from 5 to 145 ha (Davis, 2004; Helzer and Jelinski, 1999; Herkert, 1994; Walk and Warner, 1999). In some species, area sensitivity differs regionally (Johnson and Igl, 2001). Area requirements of our study species were rarely examined in urban settings. Our results show the highest occurrence probabilities for single species at 3–7 ha. In accordance with our findings, Triplet (1981) estimated the home range of crested larks at 4.6 ha. Minimum area requirements of tawny pipits in agricultural areas are 7 ha (Caplat and Fonderflick, 2009), which is in line with the threshold of 7 ha we found for urban habitats. Caplat and Fonderflick (2009) refer to wheatear and tawny pipit as ‘area-sensitive species’ (sensu Davis, 2004). Our results confirm their finding but also show that comparatively small urban wastelands seem to provide habitat for these species. 4.1.2. Vegetation and structure Vegetational variables influence species richness, abundance, and composition to a large extent (Gavareski, 1976; Melles et al., 2003; White et al., 2005). Previous studies from urban areas show that habitat quality is an essential factor for occurrence of bird species both in woodlands (Croci et al., 2008; Fahrig, 2001; Trzcinski et al., 1999) and grasslands (Haire et al., 2000). However, openland birds differ fundamentally from woodland species regarding habitat quantity, quality and connectivity. Therefore, also underlying mechanisms may differ but have not been studied as extensive as in woodlands.
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Urban matrix
Other
0.84
0.15 0.05
45%
0.25 0.10
0.25 0.10
16 %
10 % 0 1 2 3 4 Disturbance intensity
0.2
0.0 0.2 0.4 0.6 Proportion grass < 5 cm height
0.1
35 %
0.0
0.0 20 60 Proportion sealed within 200 m 0.9
0.76
0.76
0.84
0.84 0.76 0.10 13 %
0.1
0.1
9%
0.00 0.04 0.08 Proportion shrubs < 1m height 0.2
20 40 60 Proportion sealed within 2000 m 0.2
50 150 Inhabitants/ha within 2000 m
0.0 0.9
12 % 50 150 Inhabitants/ha within 2000 m
0.1
0.10
12 %
0.25
0.25
0.25
0.2
5%
24 %
0.00 0.04 Proportion grass 50-100 cm height
0.00 0.04 Proportion grass 50-100 cm height
10 20 Area size (ha)
0.00 0.04 0.08 Proportion trees < 4 m height
14 %
0.0
0.1 Proportion building
0.6
49 %
0
100 200 Inhabitants/ha within 50 m
0.1
0.1 0.0
0
100 200 Inhabitants/ha within 50 m
17 %
0.10
13 %
no yes Trees around the site
8% 0.2 0.6 Proportion sand
0.25
0.0 0.1 Proportion shrubs > 1m height
0.10 20 40 60 Proportion sealed within 2000 m
0.5
8%
0.1
0.5 31 %
0.10
0.10
15 %
0.25
20 60 Proportion sealed within 50 m 0.25
10 20 Area size (ha)
0.0 0.2 0.4 0.6 Proportion grass < 5 cm height
0.1
0.1
9%
0.25
0.0 0.5
0.5
0.0 0.1 0.2 Proportion trees > 4 m height
75 %
0.1
0.0
0.1 10 20 Area size (ha)
25 %
0.0 0.1 Proportion grass > 100 cm height
0.25
10 20 Area size (ha)
0.10
0.3
0.3
0.6
10 % 0.0 0.1 0.2 Proportion trees > 4 m height
100 200 Inhabitants/ha within 200 m
0.10
0.25 0.10
Occurence probability Occurence probability Occurence probability Occurence probability Occurence probability Occurence probability
0
56 %
0
Linnet
Grass cover
15 %
0
Wheatear
10 % 0.2 0.4 0.6 Proportion sealed within 2000 m
23 %
10 20 Area size (ha)
51 % 0
Tawny pipit
100 200 Inhabitants/ha within 200 m
13 %
0
Tree sparrow
10 20 Area size (ha)
13 % 0
Kestrel
0.84
0.15 16 % 0
Crested lark
12 % 0
0.05
0.15 0.05
Occurence probability
Red-backed shrike
10 20 Area size (ha)
Tree and shrub cover
Degree of sealing
0.76
0.84 19 % 0
0.76
0.84 0.76
Occurence probability
Inhabitants
Starling
On-site vegetation
Area size
0.0
Bird species
24 % 0.2 0.6 Proportion sand
Fig. 2. Modelled occurrence probabilities for eight Species of European Conservation concern (SPEC) in relation to predictor variables. Percentages inside each box indicate relative contribution of the variable.
Since our surveyed waste-land sites were all of an open character, the results do not show the habitat requirements in contrast to other groups such as woodland species but give a more detailed picture for open-land birds. If the demands of a species are less
specific, it comes across many wastelands, as the tree sparrow that did not respond to any on-site variables but area size. Across the eight modelled species, vegetation accounted for about one third of the explained variance. Most species responded positively to
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characteristics of early successional stages as few or no trees and shrubs, and a sparse and short grass layer. Short grass as key-habitat feature for endangered bird species is also reported from North America. From 1900 to the 1990s former common birds associated with short grass disappeared or declined there, whereas species associated with mixed and tallgrass habitats increased or held steady (Jones and Bock, 2002). Similar findings affirm the relevance of short and sparse vegetation for the crested lark in Vienna, Austria. A detailed study by Frank and Wichmann (2003) compared abandoned territories of crested larks with settled ones. Abandoned sites had less lawn, less sparse vegetated wastelands and bare soils, but more shrubs and trees, what is in line with our findings for this species. Vegetational structure seems to be crucial for habitat selection of many bird species. This has been shown for the common redstart (Phoenicurus phoenicurus; Martinez et al., 2010). As wheatear and red-backed shrike, the common redstart is a sitand-wait predator and it also declined dramatically (BirdLife International, 2004). In experiments, it favoured sparse vegetation due to higher detectability of prey, even if prey density was much higher in dense vegetation. Common redstarts assess habitat quality by using vegetation structure as a predictor of food availability, as Tye (1992) found for the wheatear. Also many other bird species prefer short vegetation for foraging (Atkinson et al., 2004). In general, decrease of short grass and sparse vegetation might be connected to application of fertilisers, less extensive grazing or mowing, or increased deposition of atmospheric nitrogen. In this respect urban areas may constitute an exception. Though the comparatively slow succession in the investigation area arises partly from sandy and nutrient-poor soils of the Berlin glacial valley, urban agglomerations may suffer less from eutrophication, since fertilisers are not used in agricultural proportions. Additionally, usual removal of topsoils on wastelands for constructions, elimination of contaminants, or pavement, reduces fertility and thus aids species of early successional stages that can grow in poor soil conditions. 4.1.3. Intrusion of humans and dogs In general, there is strong evidence that direct human disturbance by intrusion has negative impacts on bird diversity, density, and reproduction (e.g. Fernandez-Juricic et al., 2001; Flemming et al., 1988; Gutzwiller et al., 1998; Miller et al., 1998; Westmoreland and Best, 1985). Schlesinger et al. (2008) found that influence of disturbance on bird communities in forest remnants was two times higher than that of habitat loss. Many studies have found interspecific variations in the behavioural responses to human disturbance (Blumstein et al., 2005). In our study, disturbance intensity was positively correlated with occurrence of crested larks. This corresponds well with the described behaviour of this species, that is, flight distances of 1–2 m to humans and 1 m to moving cars (Glutz von Blotzheim, 1985). Explanations for this pattern could be artificial food supply, for instance in front of supermarkets, or a lower risk of predation close to humans. Neither disturbance intensity in the closer vicinity nor density and frequency of humans or dogs on-site explained any variation in the other models. Our study species either have short flight distances when approached by a human (tree sparrow, crested lark) and are thus less sensitive, or inhabit sites that were large enough to avoid encounters with humans and dogs (wheatear, tawny pipit). In contradiction to our initial hypothesis we conclude that the threatened species we investigated seem to have been able to cope with human disturbance in urban settings. The intensity of disturbance on wastelands is in general very low compared to other urban structures such as streets or parks.
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Hence, we did not display the whole gradient of disturbance but the range that can be found on wastelands. For this special kind of habitat we found no crucial role of disturbance intensity. Possibly, especially disturbance-sensitive species avoid the whole urban area and never settle on urban wastelands. Moreover, our study focussed on occurrence only, but not on reproductional success that might be influenced from other factors. 4.2. Influence of the urban matrix Our study species differed to a large extent in their response to the urban matrix in the vicinity of the study sites. Association with the degree of urbanisation covered a range from zero to 49 % of the explained variation. 4.2.1. Spatial scales Seven of the eight species modelled responded to the urban matrix at 50 m, 200 m, or multiple scales, whereas the 2000 m scale had the greatest overall influence on species’ occurrence. Also previous findings revealed that multi-level approaches are necessary for understanding response of birds to patchy systems such as urban agglomerations (Clergeau et al., 2006; Hostetler, 2001; Mazerolle and Villard, 1999; Thornton et al., 2011). The responses at different spatial scales may reflect the variation in matrix suitability among species. Habitat specialists such as wheatears (Clavero and Brotons, 2010) respond very little to the urban matrix, whereas habitat generalists as starling or tree sparrow (Clavero and Brotons, 2010) are affected by the matrix. In some cases the 2000 m buffer zones did overlap. This does not matter in a statistical way but may have strengthen some relationships at this spatial scale. 4.2.2. Human population density Three of the eight species modelled were not associated with the urban matrix (kestrel, tawny pipit, and wheatear). The remaining species were rarely found at very high human densities in the closer vicinity (linnet, tree sparrow) or at a broader scale (red-backed shrike, crested lark, starling). These species occurred more frequently in areas with densities below 80 inhabitants/ha, thus, detached houses, exclusive residential areas, or undeveloped land, partly also perimeter block developments and terraced houses (Senate Department for Urban Development, 2006). There are different possible mechanisms causing the described relationships. Overall structural diversity may be related to population density. Further, matrix features could act as criteria for habitat selection even if they do not affect birds’ fitness (Jones, 2001). Eventually, certain types of the urban matrix may cause barrier effects as shown for birds (Hodgson et al., 2007) and bats (Van Heezik et al., 2010). A special case was the starling that was likely to be found at high residential densities at the 200 m scale but avoided densely settled vicinities at the 2000 m scale. These findings possibly indicate a trade-off between advantages, such as artificial food supply, and disadvantages, such as less appropriate habitats for finding arthropods. Availability of nesting sites could also have contributed to this pattern (Hennings and Edge, 2003). 4.2.3. Degree of sealing Surface sealing had a clear influence on some species but it might affect birds indirectly because it is correlated to other land cover types such as green space. Three species that forage on the ground were rarely found at degrees of sealing beyond about 40% at the 2000 m scale. It is possible that they avoid large housing areas that are characterised by on average 38% sealed surfaces
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(Senate Department for Urban Development, 2004). Kestrels and wheatears favoured high degrees of sealing at the 200 m and 50 m scale, respectively. Both species need short vegetation or bare ground for hunting and may be attracted by sealed soils which may indicate openness, for instance parking lots or left over foundations of destructed buildings. Kestrels may also use wastelands more frequently for foraging if other open habitats are rare. 4.3. Urban wastelands Wastelands have been found to provide habitat for various groups of organisms (Angold et al., 2006; Eyre et al., 2003; Öckinger et al., 2009; Strauss and Biedermann, 2006). After Maurer et al. (2000), the most important group for nature conservation purposes within urban agglomerations are species of dry grassland communities, typical for railway areas or urban wastelands in the city. We also found a considerable number of threatened bird species on this type of habitat. The relevance of wastelands for species protection in cities becomes particularly evident if it is compared to other common forms of urban land use. Kübler (2005) explored avifauna of residential areas of Berlin along an urbanisation gradient on overall 106 ha. Out of 12 Species of European Conservation concern (SPEC) we found on wastelands, only three have been found in five types of other urban land uses, namely starlings, house sparrows, and tree sparrows. Kübler (2005) found another three threatened species that depend on woody vegetation, and thus did not occur on sparsely vegetated wastelands. Ten species were found solely on wastelands. This underlines the uniqueness of open wastelands in the range of urban land-use forms. The early successional stages of the surveyed wastelands will vanish by themselves. Thus, a dynamic cycle of spatiotemporal shifts between disturbance in terms of removal of vegetation— e.g. by mowing, grazing, or temporal use—and secondary succession could maintain open spaces and thereby increase biodiversity. These mechanisms have been shown for plants and insects on urban wastelands (Kattwinkel et al., 2009; Kleyer et al., 2007) and should be considered by urban planners (Kattwinkel et al., 2011). More research is needed for the value of urban wastelands in winter. Possibly, they are an important feeding habitat for crested lark and granivorous bird species, as well as for house and tree sparrows, that are known to suffer from lack of appropriate feeding habitats in winter (Bauer et al., 2005; Hole et al., 2002). If we take the densities of birds that breed on the wastelands (unpublished data, Meffert, 2011) and project them for the sum of all Berlin’s wastelands of about 300 ha (Senate Department for Urban Development, 2008), the following picture emerges. Wastelands provide the complete breeding habitat for the very few remaining tawny pipits (100% of estimated Berlin population of four breeding pairs; Otto and Witt, 2002) and for 100% of 115 breeding pairs of wheatears. Considerable proportions of the populations of red-backed shrikes (15% of 250), woodlarks (29 % of 85), crested larks (48% of 180), linnets (50% of 125) and skylarks (8% of 450) bred on wastelands. Of minor quantitative importance for breeding birds are those areas for starling, tree sparrow, and house sparrow. However, they seem to be attractive for foraging for breeding birds, during the post-breeding season, and also in winter. Thus, the potential of urban wastelands for providing habitat for SPEC species is high for some species at a local scale. In a wider spatial context, population numbers are not as high that they could fully compensate for changes and population declines outside urban areas, but they may help to offset the loss of grasslands on the countryside.
Moreover, wastelands could be a contribution to a more integrative approach in nature conservation that does not strictly separate between valuable protected and other areas. In this analysis, we used only survey and not reproduction data. Therefore, we cannot determine whether urban wastelands are valuable in terms of reproduction and survival. But there is initial evidence that breeding success of wheatears on wastelands seems not to be lower compared to natural habitats (Meffert et al., submitted for publication). Increasingly, our cultivated landscape does not provide significant habitat for biota and such land cover is increasing. As long as we are not able to stop this trend, protection of threatened species within urban agglomerations could partly compensate. 4.4. Implications for urban planning and nature conservation—can you imagine a park without trees? Our results show that some endangered open-land bird species inhabit urban wastelands. As unintentionally provided habitats, wastelands differ in various aspects from planned green spaces. Urban planners may use our findings for the design of green spaces to enhance biodiversity and break with our traditional image of urban green consisting of lawn and trees that not only reduces overall biodiversity, but also separates us from nature (Turner et al., 2004). To provide habitat for open-land birds, territories must be large enough. As a rule of thumb, sites above 5 ha harbour some rare bird species, those above 7 ha are especially valuable for threatened open-land bird species. To decrease disturbance levels by humans and dogs, we recommend areas exceeding 10 ha. Carefully planning of trails also can reduce disturbance to the interior or most valuable areas of the habitat. Some species can be helped by providing structures for nesting, such as piles of stones or gabions for the wheatear. With regard to vegetation, we recommend not to dissect the open space by planting trees and high shrubs. Open soils and sparse and short vegetation are of high value. Thus, we recommend to forego high woody vegetation, or at least to concentrate it in certain places on the edge of the area. In the grass layer, spontaneous vegetation should be included and potentially enriched with varied and local seeds. First examples of agricultural-like green areas in Berlin showed both high acceptance by the residents and high biodiversity (Köstler et al., 2006). In addition, predictions of climate development for the region predict less precipitation and desertification (Gerstengarbe et al., 2003). Adaption to these changes regarding the design of green areas could be used for rethinking, e.g. by avoiding woody vegetation that needs watering and including patches with open soils and sparse vegetation. Acknowledgements We thank Leonie K. Fischer and an anonymous referee for improving early drafts of the manuscript, Barbara Clucas for improving the English, and the German Research Foundation (DFG) for funding (Graduate Research Programme on Urban Ecology 780/3). Appendix A Relative contributions of the predictor variables (%) to explain the occurrence of eight bird species by boosted regression tree models. For description of variables see Table 1.
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P.J. Meffert, F. Dziock / Biological Conservation 153 (2012) 87–96 Table 1
Predictor variable
Area size Inhabitants/ha within 50 m Inhabitants/ha within 200 m Inhabitants/ha within 2000 m Proportion sealed within 50 m Proportion sealed within 200 m Proportion sealed within 2000 m Proportion trees < 4 m height Proportion trees > 4 m height Proportion shrub < 1 m height Proportion shrub > 1 m height Proportion grass < 5 cm height Proportion grass 5–10 cm height Proportion grass 50–100 cm height Proportion grass > 100 cm height Proportion moss Trees around the site Proportion sealed Proportion of sand Disturbance intensity Proportion building
Model Crested lark
Kestrel
Linnet
Red-backed shrike
Starling
Tawny pipit
Tree sparrow
Wheatear
13.0 0.0 0.0 5.4 6.1 0.0 12.4 0.0 7.0 9.4 0.0 16.4 6.7 0.0 8.6 5.1 0.0 0.0 0.0 10.0 0.0
13.2 0.0 0.0 0.0 0.0 12.8 0.0 35.0 0.0 0.0 17.6 0.0 0.0 0.0 0.0 0.0 0.0 7.3 0.0 0.0 14.1
0.0 15.3 0.0 0.0 0.0 0.0 30.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0 16.6 0.0 13.0 0.0 24.3 0.0 0.0
15.7 0.0 23.3 16.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 44.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0
19.2 0.0 11.7 12.0 0.0 0.0 9.5 5.0 9.9 0.0 0.0 8.6 0.0 24.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
56.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 14.8 0.0 0.0 25.0 0.0 4.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0
50.6 49.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
75.2 0.0 0.0 0.0 9.0 0.0 0.0 0.0 0.0 0.0 7.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 8.1 0.0 0.0
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