Urbanization induces bird color homogenization

Landscape and Urban Planning 192 (2019) 103645

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Urbanization induces bird color homogenization

T

Lucas M. Leveau Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires – IEGEBA (CONICET – UBA), Ciudad Universitaria, Pab 2, Piso 4, Buenos Aires 1426, Argentina

A R T I C LE I N FO

A B S T R A C T

Keywords: Birds Human perception Land-use Null models Plumage color Traits

Urbanization acts as an environmental filter that allows bird species with certain ecological traits, such as a generalist diet and nesting on buildings, to occur in urban centers. However, its effect on other bird traits, such as plumage color, has still not been studied. The aim of this study was to analyze changes in plumage diversity and composition along urbanization gradients of three cities in central Argentina: Mar del Plata, Balcarce and Miramar. Bird surveys were made in urban, suburban and rural areas using transects during two breeding seasons. Color description and bird size were obtained from the literature. Color diversity was calculated using functional diversity indices: FD and FDis. Null models that control for species richness were used to estimate standardized effect sizes. Color composition was analyzed using Non-metric multidimensional scaling. FD and FDis decreased with percentage of impervious cover and increased with habitat diversity, whereas FDis also showed an interaction between city type and impervious cover. After both indices were controlled for species richness, they showed decreases with impervious cover and effects of city type. Highly urbanized areas were dominated by grey color, plumage dimorphism, polymorphism and small and medium sizes. Sites with high habitat diversity were inhabited by species of yellow and green coloration, whereas rural areas were occupied by large species with combinations of black, brown and white. More urbanized areas show not only fewer species, but also species that look more similar than expected by chance. These results suggest that urbanization acts as an environmental filter for bird colors, allowing the presence of birds with similar colors.

1. Introduction Urbanization is the most abrupt change of natural and seminatural ecosystems, affecting several facets of bird diversity, such as taxonomic, functional and phylogenetic diversities (Ibáñez-Álamo, Rubio, Benedetti, & Morelli, 2017; La Sorte et al., 2018; Morelli et al., 2016, 2017; Oliveira Hagen, Hagen, Ibáñez-Álamo, Petchey, & Evans, 2017; Sol, Bartomeus, González-Lagos, & Pavoine, 2017). Highly urbanized areas induce a reduction in the number of species, their ecological functions and their evolutionary uniqueness (Evans, Reitsma, Hurlbert, & Marra, 2018; La Sorte et al., 2018; Morelli et al., 2016). Although some reports show that moderate or low levels of urbanization have values of taxonomic and functional diversity similar to or higher than those in natural and seminatural areas (Blair, 1996; Bock, Jones, & Bock, 2008; Leveau & Leveau, 2005; Oliveira Hagen et al., 2017), urbanization impacts on species composition are significant (SuarezRubio, Leimgruber, & Renner, 2011). Urban areas act as an environmental filter that allow the occurrence of bird species with certain life-history traits: small size, diet generalists, gregarious behaviour, resident and tree- or building-nesting (Blair & Johnson, 2008; Callaghan et al., 2019; Croci, Butet, & Clergeau,

2008; Evans et al., 2018; Jokimäki, Suhonen, Jokimäki-Kaisanlahti, & Carbó-Ramírez, 2016; Kark, Iwaniuk, Schalimtzek, & Banker, 2007; Leveau, 2013). Moreover, there is a phylogenetic filter, since urban areas have a greater proportion of species classified as Passeriforms, Columbiforms and Psittaciforms than the surrounding non-urban areas (La Sorte et al., 2018). In addition, other traits such as plumage color may be important in determining their ability to thrive in urban areas. Along urbanization gradients, environmental colors vary from grey in areas dominated by impervious cover to green in suburban and exurban areas dominated by scattered houses and yards. These environmental differences may interact with plumage colors, determining intraspecific communication or predation risk (Barreira & García, 2019; Delhey & Peters, 2017; Marchetti, 1993). Bird color variation was analyzed mainly at large geographical scales, and studies found a positive relationship of color diversity and brightness with the amount of resources and habitat structure (Dalrymple et al., 2018; Delhey, 2018; McNaught & Owens, 2002). A large quantity and variety of resources may mean a wider variety of nutrients and may provide better resource conditions for the expression of vibrant coloration (Dalrymple et al., 2018). According to the dominant color of the environment, birds may use their plumage color to

E-mail address: [email protected]. https://doi.org/10.1016/j.landurbplan.2019.103645 Received 29 January 2019; Received in revised form 17 July 2019; Accepted 21 August 2019 0169-2046/ © 2019 Elsevier B.V. All rights reserved.

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protect from predators. For example, habitats with greater vegetation cover may favour the presence of green plumage birds, enhancing crypsis (Delhey, 2018; Friedman and Remeš 2017; Kamilar & Bradley, 2011). Alternatively, the presence of more luminant visual signals, such as yellow, may favour intraspecific bird communication in shaded environments (Dalrymple et al., 2018; Endler 1978, 1993). Along urbanization gradients, highly urbanized areas dominated by impervious surfaces would be inhabited by bird species of grey color, which favours crypsis. In addition, less urbanized areas with more habitat diversity would be inhabited by bird species with increased color diversity, which enables different crypsis strategies given the variety of color substrates. Moreover, the enhanced variety of resources in suburban and rural areas may provide nutrients that help the expression of a greater variety of colors than in urban centers dominated by impervious surfaces. If local assemblages are composed of random sets of species, a positive relationship between species richness and color diversity is expected because the addition of new species will probably add new colors to the assemblage. For example, highly urbanized areas, which are generally inhabited by few species, are expected to have a lower color diversity than richer suburban areas (Leveau, 2019). Non-random distributions of species’ colors suggest that certain processes, such as limiting similarity or environmental filtering, structure local assemblages (Holdaway & Sparrow, 2006; Petchey, Evans, Fishburn, & Gaston, 2007). Different hypotheses of community assembly can be tested by comparing observed values of color diversity to those obtained from simulated bird assemblages for a given number of species (Petchey et al., 2007) (Fig. 1). For instance, highly urbanized areas may be inhabited by a few species with more similar colors than expected by chance, indicating that urbanization is an environmental filter for bird plumage colors. Several reports have shown a positive relationship between bird species richness and human well-being in cities, which is called the feelgood factor (Fuller, Irvine, Devine-Wright, Warren, & Gaston, 2007; Dallimer et al., 2012; Carrus et al., 2015; Wheeler et al., 2015, but see Shwartz, Turbé, Simon, & Julliard, 2014). Humans perceive bird species through bird songs, size or plumage colors (Garnett, Ainsworth, & Zander, 2018; Lišková, Landová, & Frynta, 2015). Indeed, the variety of

Table 1 Final models of the relationship of diversity of plumage colors and bird size with environmental variables along three urbanization gradients in central Argentina. Asterisks indicate interaction between environmental variables. In the case of categorical variables and their interaction with continuous variables, Balcarce and Impervious*Balcarce are in the intercepts. Bold P values are significant. SE: standard error. Diversity index

Estimate

SE

t value

P

r2

a) FD Intercept Percent impervious cover Habitat diversity (H′)

2.17 −0.03 13.44

1.15 0.01 2.47

1.89 −3.81 5.44

0.066 0.000 0.000

0.54

−0.29 0.00 0.41 −0.39 −0.02 −0.00

0.30 0.01 0.44 0.45 0.01 0.01

−0.95 −0.55 0.94 −0.87 −3.24 −0.65

0.346 0.584 0.352 0.388 0.002 0.517

0.51

0.36 −0.00 0.05 −0.02 0.30 −0.00 0.00

0.03 0.00 0.03 0.03 0.06 0.00 0.00

10.90 −4.18 1.60 −0.80 4.93 −0.64 2.10

0.000 0.000 0.119 0.430 0.000 0.524 0.042

0.69

0.12 −0.01 0.59 −0.04

0.22 0.00 0.27 0.27

0.53 −2.74 2.21 −0.17

0.600 0.009 0.033 0.867

0.26

b) FD SES Intercept Impervious percent cover Mar del Plata Miramar Impervious*Mar del Plata Impervious*Miramar c) FDis Intercept Impervious percent cover Mar del Plata Miramar Habitat diversity (H′) Impervious*Mar del Plata Impervious*Miramar d) FDis SES Intercept Impervious percent cover Mar del Plata Miramar

bird songs has been correlated with the well-being of people (Hedblom, Heyman, Antonsson, & Gunnarsson, 2014), and Belaire, Westphal, Whelan, and Minor (2015) found that aesthetic aspects of birds were the most valuable. Therefore, considering urban planning, it is important to know how urbanization affects the variety of bird songs or visual characteristics of birds. To my knowledge, the effect of urbanization on interspecific bird color diversity and composition has still not been studied. Here, I examine the interspecific variation and composition of bird colors along urbanization gradients located in three cities of central Argentina. Given that urbanization gradients vary according to the percentage of impervious cover, habitat diversity and vegetation type, it is expected that: 1) the areas with greater vegetation cover and greater habitat diversity will have greater color diversity; 2) color diversity will be lower than expected by chance in the most urbanized areas, indicating that urbanization is an environmental filter on bird colors; and 3) according to the crypsis hypothesis, dominant bird colors should match the dominant colors of the local environment. 2. Methods 2.1. Study area The study was carried out in three cities of the Pampas region, in Buenos Aires province (Argentina): Mar del Plata (615 350 inhabitants), Balcarce (38 823 inhabitants) and Miramar (29 629 inhabitants) (2010 National census). The maximum distance between cities was 59 km (between Balcarce and Miramar); thus, the effects of latitude or climate were minimal. The landscape surrounding the cities is characterized by cropland, pastureland, grasslands and exotic tree plantations. The climate is temperate, with mean annual temperature of 14 °C and mean annual precipitation of 923.6 mm (data from the

Fig. 1. Hypothetical relationships between color diversity and species richness for assemblages composed of random sets of species (black line). Non-random assemblages with high color diversity for their given level of species richness contain species that are more dispersed in color values than expected by chance, indicating a limiting similarity process among species. Non-random assemblages with low color diversity for their given level of species richness contain species that have more similar colors than expected by chance, indicating an environmental filtering process. 2

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Fig. 2. Relationships of color diversity (FD) with a) percent impervious cover, and b) habitat diversity (H′); and relationship of standardized effect size (SES) of FD with (c) percent impervious cover in three cities of central Argentina. The red line represents the fitted line and the grey areas are the confidence intervals at 95%.

from the Aves Argentinas free mobile phone application, both consulted during January 2019. Color types were taken from 12 patches of bird body (Table S1, Supplementary information): 1) crown, 2) head, 3) cheek, 4) mantle, 5) primaries, 6) wing coverts, 7) back, 8) rump, 9) tail, 10) belly, 11) breast, and 12) throat. When the rump color description was not available, it was replaced with photographs from Google. I created binary categories for body patches that had two colors, where the first color was the dominant. For example, the primaries of the European Greenfinch (Chloris chloris) were characterized as grey_yellow because they were predominantly grey, with some yellow. Also, I considered four plumage and bird characteristics (Table S1, Supplementary information): 1) whether species had sexual dimorphism; 2) whether they were polymorphic, as in the case of the Rock Dove (Columba livia); 3) percentage of iridescent plumage; and 4) body size, from the Handbook of the Birds of the World.

Meteorological National Service). 2.2. Bird surveys Bird surveys were carried out in three habitat types: 1) urban center; 2) suburban areas composed of detached houses with yards; and 3) rural areas, composed of crops and pastures (see Leveau, 2019 for details). The urban center was the main commercial and historical part of the city, which is characterized by a central urban park of 3–4 ha surrounded by buildings. Suburban areas were located using Google Earth, and rural areas were at least 1 km from the city fringe, adjacent to secondary roads. In each habitat I placed five 100 × 50-m transects separated by at least 200 m from one another. During each breeding season, corresponding to the 2011–2012 and 2012–2013 austral springsummer, transects were visited twice, totalling four visits to each transect. Surveys were carried out in the first 4 h after dawn on days without rain or strong winds, and all birds seen or heard were counted, except those flying over the top of buildings or trees, or below that height but showing no feeding activity.

2.4. Color diversity and composition The table of color characteristics was used to calculate a dissimilarity distance among species, employing the Gower distance, which can handle numerical and categorical data. The function gowdis of the FD package in R was used (Laliberté, Legendre, Shipley, & Laliberté, 2015; R core Team, 2017). With this dissimilarity values, two diversity indices originally proposed for functional diversity, were calculated: FD, based on presence/absence data of species (Petchey & Gaston, 2002), and functional dispersion (FDis, Laliberté & Legendre, 2010),

2.3. Bird coloration A matrix was created with plumage characteristics as columns and bird species as rows (Table S1, Supplementary information). Male plumage description, plates and photographs were taken from the Handbook of the Birds of the World Alive (https://www.hbw.com) and 3

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Fig. 3. Relationship of plumage color diversity considering species abundances (FDis) with a) percent impervious cover in three cities of central Argentina, and b) habitat diversity (H′); and relationship of standardized effect size (SES) of FDis with c) percent impervious cover, and d) city. The red line represents the fitted line and the grey areas are the confidence intervals at 95%.

which considers the relative abundances of species. On the one hand, FD (Petchey & Gaston, 2002) is based on a dendrogram of bird species color characteristics and measures the total branch length of species present in a given transect. Therefore, a dendrogram was constructed with the Unweighted Pair Group Method with Arithmetic Mean, which resulted in the best cophenetic correlation between the dissimilarity matrix and the distance between species in the dendrogram. The function hclust of the stats package in R was used for hierarchical clustering, and the function treedive of the vegan package (Oksanen et al., 2017) was used to calculate FD for each transect. On the other hand, FDis is the mean distance in the multidimensional trait space of individual species to the centroid of all species (Laliberté & Legendre, 2010). The multidimensional space is obtained through a principal coordinate analysis from the Gower dissimilarity matrix. FDis, unlike FD, can account for relative abundances of species, and the position of the centroid in the multidimensional space will shift toward the most abundant species. Color diversity indices can be positively correlated to species richness because a random addition of species may result in an increase of color types (Dalrymple et al., 2018). Therefore, the observed indices were compared with null distributions by reshuffling species 999 times. Null models were obtained from Swenson (2014), using the richness method for FD and the independent swap method for FDis in the picante package of R (Kembel et al., 2010). Observed and expected diversity values were compared by calculating a standardized effect size index (SES):

Fig. 4. Non-metric Multidimensional Scaling (Stress = 0.15) for predominant colors in bird species, frequency of plumage dimorphism, polymorphism, iridescence, and size ranges, and their relationship with percent impervious cover and habitat diversity (H′). The blue arrows show the direction of the environmental gradient, with arrow length being proportional to the correlation between the environmental variable and the ordering of the NMDS (Oksanen, 2015). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

4

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SES = Observed diversity value − mean null diversity values/standard deviation of null diversity values A total of 999 null values were calculated. Positive and negative SES values indicate that the diversity of colors is greater and lower than expected for a given number of bird species, respectively. Negative SES values are compatible with environmental filtering inducing color convergence, whereas positive SES values are compatible with effects of trait divergence (Petchey et al., 2007). The influence of urbanization on color composition was assessed by classifying each species according to their dominant color, sexual dimorphism, polymorphism, presence of iridescence, and size. The most represented color in the different body parts analyzed was regarded as the dominant color (see Table S1, Supplementary material). Size was assigned to one of three categories considering the length data of the observed species: small (10 to 24 cm), medium (24 to 39 cm), and large (39 to 53). Then, a matrix of species and the number of individuals for each color type was used to calculate Bray-Curtis dissimilarity indices among transects. Non-metric multidimensional scaling (NMDS) was performed with the function metaMDS in the vegan package (Oksanen et al., 2017). Finally, to identify the plumage traits associated with the different environmental variables, NMDS axis were related to impervious cover percentage, habitat diversity and city type using the function envfit in vegan.

relationship with habitat diversity (Table 1, Fig. 2a, b). However, after accounting for species richness, FD SES was not related to habitat diversity and varied its response to impervious cover among cities (Table 1, Fig. 2c). The sharpest decline of FD SES with impervious cover was recorded in the largest city, Mar del Plata. FDis had a positive response to habitat diversity and its relationship with impervious cover varied among cities (Table 1, Fig. 3a, b). The declines of FDis were sharper in Mar del Plata and Balcarce than in Miramar. After accounting for species richness, FDis SES showed a negative response to impervious cover and varied among cities, being highest in Mar del Plata (Table 1, Fig. 3c, d). Bird color composition varied according impervious cover and habitat diversity (Fig. 4). Sites dominated by impervious surfaces were inhabited by grey bird species, more presence of iridescence, polymorphism and sexual dimorphism. Sites with high habitat diversity and percent cover of trees, lawn and shrubs were inhabited by species characterized by green-yellow or black-blue combinations (Fig. 4). Sites with the smallest impervious cover and dominated by crops and nonmanaged herbaceous vegetation exhibited more abundance of large individuals with black, brown-white combination, and black-brown combination.

2.5. Urbanization and habitat diversity

The results obtained indicate that highly urbanized areas have led to a reduction of bird color types. As a result of increasing impervious areas, there is a decrease of vegetation cover and the quantity and variety of food resources and nutrients that help to the expression of bird plumage coloration, as suggested by Dalrymple et al. (2018). Furthermore, the results showed that the diversity of colors in birds may increase in suburban areas with high habitat heterogeneity. When species richness was considered (SES values), the role of habitat heterogeneity became non-significant, indicating that its effect on color diversity was mediated by an increase in the number of bird species. Moreover, the negative effect of urbanization on color diversity persisted, suggesting that urbanization acts as an environmental filter on bird color types. Indeed, grey bird species were dominant in highly urbanized areas. The effect of impervious cover on color diversity varied with city, suggesting that city size may have a role in the diversity of bird colors. For example, the stronger impact of impervious cover on FD SES was recorded in the largest city (Mar del Plata), where urban and suburban areas have a greatest distance to non-urban areas and the car and pedestrian traffic are the highest (L. Leveau, unpublished data). Thus, human disturbance and isolation may impose environmental filters of bird color types. In the case of FDis SES, which considered bird abundance and took into account species richness, the largest city had a greater diversity of colors than Balcarce and Miramar. Given that city area size has a positive influence on the number of species (MacGregorFors, Morales-Pérez, & Schondube, 2011), urban and suburban areas of Mar del Plata likely had the greatest influx of bird individuals with different number of colors of the three cities, and that influx would be even in terms of species abundance. Bird color composition varied along the urbanization gradients, from grey in the most urbanized areas to combinations of brown, black and white in rural areas. These patterns may be related to adaptations of species to different background colors or light environment (Endler, 1993; McNaught & Owens, 2002). Bird species of urban centers, such as the House Sparrow, the Rock Dove and the Eared Dove, are mainly grey; this coloration is in low contrast to impervious surfaces and may provide effective crypsis against predators. In rural areas, where unmanaged herbaceous vegetation and crops may have brown shades, there is a low contrast with species with combinations of brown, white and black, such as the Red-winged Tinamou (Rhynchotus rufescens) and the Firewood-gatherer (Anumbius annumbi). On the other hand, bird species can increase conspicuousness by having contrasting colors in

4. Discussion

Habitat structure was measured in two 25-m radius circles located in each transect, one in the center of the first 50 m along transects and the other in the center of the remaining 50 m. In each circle, the percent cover of the following substrates were estimated visually: 1) trees, 2) shrubs, 3) lawn (managed herbaceous vegetation), 4) buildings, 5) nonmanaged herbaceous vegetation, 6) cultivated land, and 7) paved roads. Percent cover of buildings and paved roads was summed to obtain a measure of impervious surface cover in each circle and then averaged values of both circles in each transect. On the other hand, habitat diversity in each transect was estimated using the Shannon index, which incorporated the percent cover of trees, shrubs, lawn, herbaceous vegetation, cultivated land and buildings. When the percent cover of habitat components exceeded 100%, values were corrected for up to 100%. Habitat diversity was highly correlated with percent cover of trees (Pearson correlation, r = 0.65), lawn (r = 0.71), and shrubs (r = 0.68), whereas impervious cover was negatively correlated with percent cover of crops (r = −0.82) and non-managed herbaceous vegetation (r = −0.84). 2.6. Statistical analysis Generalized linear models with a Gaussian distribution of errors were used to analyze the relationship between color diversity measures, their SESs and the environmental variables (habitat diversity and impervious cover); city was considered a categorical factor. The whole models included the interactions between impervious cover and city, and between habitat diversity and city. The final models were obtained by excluding non-significant variables (P > 0.05) through Likelihood ratio tests (LRT). Pseudo-R2 of models were calculated using the McFadden (1973) formula: Pseudo-R2 = 1 − (Residual deviance/Null Deviance). Models were plotted using the visreg package (Breheny & Burchett, 2013). 3. Results A total of 54 species and 2200 individuals were counted. The most abundant species were the House sparrow (Passer domesticus, 27% of individuals), the Eared Dove (Zenaida auriculata, 14%) and the Rock Dove (Columba livia, 12%). FD showed a negative response to impervious cover and a positive 5

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species, but also species that look more similar than expected by chance. However, the effect of impervious surface cover on color diversity changed with city, suggesting that the role of city size deserves further research. In addition, plumage colors were related to the predominant colors of the different environments, likely to enhance crypsis. Therefore, the new habitats created along the urbanization gradients may impose different levels of predation risk (Delhey & Peters, 2017). For instance, a Rock Dove individual may be more conspicuous to a raptor eye on lawn than on a paved surface. In short, plumage color is another bird trait that should be included in the characterization of bird adaptations to urban areas. Considering the human preferences in bird plumage color and size, intermediate levels of urbanization seem to favour yellow birds, but large birds were generally absent from cities. However, the results obtained in this study should be compared with other biomes that have different regional pools of species.

comparison to the environment and enhancing the intraspecific communication (Dalrymple et al., 2018; Endler, 1978). For instance, species whose dominant color is yellow, such as the Saffron Finch (Sicalis flaveola) and the Hooded Siskin (Spinus magellanica), were more abundant in suburban areas, where they contrast with the green habitat dominated by lawn, shrubs and trees. Intraspecific variation in bird color was predominant in highly urbanized areas. The high densities of urban exploiters were related to the highest abundance of polymorphism in the case of the Rock Dove, and dimorphism in the case of the Eared Dove and the House Sparrow. On the one hand, polymorphism in the Rock Dove is related to individual variations in breeding success and immune responses to endoparasites, driven by genetic differences (Jacquin, Lenouvel, Haussy, Ducatez, & Gasparini, 2011; Murton, Thearle, & Coombs, 1974). Furthermore, Galeotti, Rubolini, Dunn, and Fasola (2003) suggested that plumage polymorphism evolved as a response to diurnal activity extension to night or vice versa, and to different detectability under variable light conditions. Indeed, the Rock Dove has been shown to have nocturnal activity in several cities (Leveau, 2018). On the other hand, plumage dimorphism is more likely among granivorous species with carotenoidpoor diets; in these species, acquiring carotenoids could be considered an honest signal of male quality (Croci et al., 2008; Gray, 1996). Indeed, the House Sparrow and the Eared Dove are granivorous species that were very abundant in the urban centers of the three studied cities. Our results disagree with the pattern found by Croci et al. (2008), who reported that urban adapters had a lower occurrence of plumage dimorphism than urban avoider species. Moreover, Kark et al. (2007) did not find differences in sexual dimorphism between urban and nonurban species in Israel. Discrepancies among studies may be due to different spatial scales used or dissimilarities in the regional pool of species. Color type and life-history traits of bird species were probably interrelated in their responses to urbanization. Bird species of highly urbanized areas and generally grey colors, such the Rock Dove and the House Sparrow, also have similar diets and nesting sites, which allow them to thrive there (Leveau, 2013). However, green bird species that inhabit areas dominated by trees, shrubs and lawn, such as the Whitethroated Hummingbird (Leucochloris albicollis) and the Monk Parakeet (Myiopsitta monachus), have different diets (nectarivorous and granivorous, respectively). Therefore, further analyzes that discriminate the effect of life-history traits from that of color type are needed. Plumage color and body size have been shown to be important visual characteristics that humans can perceive in birds (Garnett et al., 2018; Lišková et al., 2015). Large size and blue and yellow colors were appreciated in experiments and correlational studies (Su, Cassey, VallLlosera, & Blackburn, 2015; Lišková et al., 2015; Correia, Jepson, Malhado, & Ladle, 2016; Garnett et al., 2018). Along our urbanization gradients, blue and yellow colors in bird plumage were present in suburban areas. However, large-sized birds were almost absent from urban and suburban areas. These types of birds are affected by the presence of humans due to their longer flight initiation distances than smaller species (Møller, 2012; Morelli et al., 2018). Given that this study was focused on the interaction between plumage color, the environment and human perception, I used plumage color descriptions. However, studies that focused mainly on bird intraspecific and interspecific interactions used more objective measures of plumage reflectance obtained from bird skins in museums or bird plates from books (Barreira & García, 2019; Dale, Dey, Delhey, Kempenaers, & Valcu, 2015; Delhey, 2018). Therefore, the present results should be considered with caution.

Acknowledgements I thank Jorgelina Brasca and Victoria Eusevi for the improvement of the English writing. Christopher Lepczyk and two anonymous reviewers helped to improve a first draft of the manuscript. Bird silhouettes were taken from silhouettegardem.com. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.landurbplan.2019.103645. References Barreira, A. S., & García, N. C. (2019). Visual and acoustic communication in Neotropical birds: Diversity and evolution of signals. Behavioral Ecology of Neotropical Birds (pp. 155–183). Cham: Springer. Belaire, J. A., Westphal, L. M., Whelan, C. J., & Minor, E. S. (2015). Urban residents’ perceptions of birds in the neighborhood: Biodiversity, cultural ecosystem services, and disservices. The Condor, 117(2), 192–202. Blair, R. B. (1996). Land use and avian species diversity along an urban gradient. Ecological Applications, 6(2), 506–519. Blair, R. B., & Johnson, E. M. (2008). Suburban habitats and their role for birds in the urban–rural habitat network: Points of local invasion and extinction? Landscape Ecology, 23(10), 1157–1169. Bock, C. E., Jones, Z. F., & Bock, J. H. (2008). The oasis effect: Response of birds to exurban development in a southwestern savanna. Ecological Applications, 18(5), 1093–1106. Breheny, P., Burchett, W. (2013). Visualizing regression models using visreg. < http:// myweb.uiowa.edu/pbreheny/publications/visreg.pdf/ > . Callaghan, C. T., Major, R. E., Wilshire, J. H., Martin, J. M., Kingsford, R. T., & Cornwell, W. K. (2019). Generalists are the most urban-tolerant of birds: A phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization. Oikos. Carrus, G., Scopelliti, M., Lafortezza, R., Colangelo, G., Ferrini, F., Salbitano, F., ... Sanesi, G. (2015). Go greener, feel better? The positive effects of biodiversity on the wellbeing of individuals visiting urban and peri-urban green areas. Landscape and Urban Planning, 134, 221–228. Correia, R. A., Jepson, P. R., Malhado, A. C., & Ladle, R. J. (2016). Familiarity breeds content: Assessing bird species popularity with culturomics. PeerJ, 4, e1728. Croci, S., Butet, A., & Clergeau, P. (2008). Does urbanization filter birds on the basis of their biological traits? The Condor, 110(2), 223–240. Dale, J., Dey, C., Delhey, K., Kempenaers, B., & Valcu, M. (2015). The effects of lifehistory and social selection on male and female plumage coloration. Nature, 527, 367–370. Dallimer, M., Irvine, K. N., Skinner, A. M., Davies, Z. G., Rouquette, J. R., Maltby, L. L., ... Gaston, K. J. (2012). Biodiversity and the feel-good factor: Understanding associations between self-reported human well-being and species richness. BioScience, 62(1), 47–55. Dalrymple, R. L., Flores-Moreno, H., Kemp, D. J., White, T. E., Laffan, S. W., Hemmings, F. A., ... Moles, A. T. (2018). Abiotic and biotic predictors of macroecological patterns in bird and butterfly coloration. Ecological Monographs, 88(2), 204–224. Delhey, K. (2018). Darker where cold and wet: Australian birds follow their own version of Gloger's rule. Ecography, 41(4), 673–683. Delhey, K., & Peters, A. (2017). Conservation implications of anthropogenic impacts on visual communication and camouflage. Conservation Biology, 31(1), 30–39. Endler, J. A. (1978). A predator’s view of animal color patterns. Evolutionary Biology (pp. 319–364). Boston, MA: Springer. Endler, J. A. (1993). The color of light in forests and its implications. Ecological

5. Conclusions Urbanization induces homogenization of bird colors and size, favouring the establishment of small and medium-sized grey birds in highly urbanized areas. More urbanized areas show not only fewer 6

Landscape and Urban Planning 192 (2019) 103645

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