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Urban landscape organization is associated with species-specific

traits in European birds

Juan Diego Ibáñez-Álamo, Lucía Izquierdo, Emeline Mourocq,

Yanina Benedetti, Marja-Liisa Kaisanlahti-Jokimäki, Jukka
Jokimäki, Federico Morelli, Enrique Rubio, Tomás Pérez-
Contreras, Philipp Sprau, Jukka Suhonen, Piotr Tryjanowski,
Mario Díaz

PII: S0048-9697(23)06564-6
DOI: https://doi.org/10.1016/j.scitotenv.2023.167937
Reference: STOTEN 167937

To appear in: Science of the Total Environment

Received date: 18 April 2023

Revised date: 16 October 2023
Accepted date: 17 October 2023

Please cite this article as: J.D. Ibáñez-Álamo, L. Izquierdo, E. Mourocq, et al., Urban
landscape organization is associated with species-specific traits in European birds, Science
of the Total Environment (2023), https://doi.org/10.1016/j.scitotenv.2023.167937

This is a PDF file of an article that has undergone enhancements after acceptance, such
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© 2023 Published by Elsevier B.V.

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Urban landscape organization is associated with species-

specific traits in European birds

Juan Diego Ibáñez-Álamoa, Lucía Izquierdoa, Emeline Mourocqb, Yanina Benedettic,

Marja-Liisa Kaisanlahti-Jokimäkid, Jukka Jokimäkid, Federico Morellic,e, Enrique Rubioa,
Tomás Pérez-Contrerasa, Philipp Sprauf, Jukka Suhoneng, Piotr Tryjanowskih, Mario
Díazi

a. Department of Zoology, Faculty of Sciences, University of Granada, E-18071

Granada, Spain
b. Giving Life To Data-Biostatistics Analysis Services, Les Fournels, FR-34390
Prémian, France

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c. Czech University of Life Sciences Prague, Faculty of Environmental Sciences,
Kamýcká 129, CZ-165 00 Prague 6, Czech Republic

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d. Nature Inventory and EIA-Services, Arctic Centre, University of Lapland, P. O. Box
122, FI-96101 Rovaniemi, Finland
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e. Institute of Biological Sciences, University of Zielona Góra, Prof. Z. Szafrana St. 1,
PL-65-516 Zielona Góra, Poland
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f. Department of Biology, Ludwig-Maximilians-University Munich, Großhaderner Str. 2
82152 Planegg-Martinsried, Germany
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g. Department of Biology, University of Turku, Turku, Finland

h. Department of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C,
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PL-60-625 Poznań, Poland

i. Department of Biogeography and Global Change, Museo Nacional de Ciencias
Naturales (BGC-MNCN-CSIC), E-28006 Madrid, Spain ORCID 0000-0002-6384-6674
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Corresponding author: J.D. Ibáñez-Álamo (e-mail: jia@ugr.es; phone: +34

958243243)

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1. Introduction

Human-induced land-use changes are one of the main drivers of current

terrestrial biodiversity loss (Newbold et al., 2015). Among these changes, urbanization

has become one of the most important threats to biodiversity (Grimm et al., 2008; Seto

et al., 2012). More than half of the human world population now lives in cities, a trend

that is speeding up (United Nations, 2019). This human pressure can have important

negative impacts on ecosystems through habitat loss or fragmentation, such as loss of

biodiversity (Li et al., 2022; McKinney, 2008; Piano et al., 2020). Multiple studies have

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shown that cities are associated with reduced levels of taxonomic biodiversity

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(Callaghan et al., 2021; Fenoglio et al., 2020), although there is no consensus on how
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urbanization affects functional (Oliveira Hagen et al., 2017; Sol et al., 2020; Villalta et

al., 2022) and phylogenetic diversity (Morelli et al., 2016; Villalta et al., 2022). Cities are
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known to filter certain species inducing a process of biotic homogenization (Devictor et
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al., 2008; Ibáñez-Álamo et al., 2017; McKinney, 2008; Sol et al., 2020). This selection

acts mainly through the biological traits of organisms (Croci et al., 2008; Jung and
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Threlfall, 2018) with some species filtered out from urban areas (i.e. urban avoiders)

while others being able to exploit these new habitats (i.e. urban exploiters and
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suburban adapters) (Blair, 1996). The species-specific traits allowing animals to inhabit
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urban landscapes are well-studied for birds (Callaghan et al., 2019; Croci et al., 2008;

Evans et al., 2011; Jokimäki et al., 2016; Møller & Díaz 2017; Sol et al., 2014). Several

investigations have pointed out that urban tolerant species tend to be generalist in

ecological traits such as habitat selection or foraging behaviour (Callaghan et al., 2020,

2019), and are also characterized by morphological traits such as smaller body size

(Neate-Clegg et al., 2023), life-history traits such as fecundity or productivity (e.g.,

larger clutch size but a lower number of breeding attempts per year) (Croci et al., 2008;

Evans et al., 2011; Neate-Clegg et al., 2023), or even social traits such as parental

care (Croci et al., 2008; Kark et al., 2007). On the other hand, urban avoiders are

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associated with other set of traits (e.g. specialism in terms of foraging or nesting

preferences) (Callaghan et al., 2020, 2019). These highlighted traits are directly linked

to urban landscape characteristics (especially vegetation attributes) ultimately

determining species responses to urbanization (Dale, 2018; Ikin et al., 2012; Jokimäki

et al., 2016). This implies that urban landscape attributes and how urban areas expand

can have an important role in shaping urban bird communities.

Cities are landscape mosaics composed of patches ranging from natural

remnants of vegetation or green spaces to residential areas, industrial or commercial

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zones, whose spatial configuration shows clear-cut differences depending on their

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design (Forman, 2014). This heterogeneity produces many microhabitats and new

niche opportunities which can have a relatively high value for biodiversity (Forman,
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2014). Although the form in which cities sprawl is variable, urban areas can be
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arranged in the following urban development types : land-sharing and land-sparing
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areas that are the two extremes of a gradient (Lin and Fuller, 2013). Land-sparing

implies highly urbanized areas with high density housing (e.g. multi-story buildings),
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high population density and large green areas (e.g., parks). In contrast, land-sharing

implies extensive areas characterized by low-density housing (e.g., single-family

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houses), low population density and fragmented small green areas (e.g. gardens or
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street vegetation). These two types of urban development are associated with

differences in biodiversity (Ibáñez-Álamo et al., 2020; Lin and Fuller, 2013; Soga et al.,

2014) suggesting the possibility of a specific set of traits that allow some species to

tolerate better either land-sharing or land-sparing urban development types. For

instance, land-sparing (with large and unfragmented green patches, sometimes

remnants of native forest) could benefit human-sensitive forest species (Gagné and

Fahrig, 2010; Sushinsky et al., 2013), thus maintaining a higher number of rare species

with more specialized traits and less urban tolerance (Suhonen et al., 2022). However,

these studies did barely address the mechanisms underlying this potential filtering

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effect. One suggested mechanism implies changes in predation pressure. Land-

sharing urban areas seem to have higher nest predation pressure than land-sparing

areas (Jokimäki et al., 2020), thus having the potential to select species based on the

susceptibility of certain nest types to predation. To our knowledge, studies that have

investigated this association between the urbanization process and species-specific

traits are focused on the rural-urban context rather than trying to explore this question

within the urban matrix (i.e. regarding urban development types).

In our study, we investigate whether urban development type (i.e. land-sharing

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or land-sparing) is associated with a particular set of species-level traits (morphological,

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ecological, social or life-history characteristics) using birds from multiple European

cities as our model system. We hypothesized that differences in green area

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fragmentation between urban development types would have an important role in this
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context. We predicted that land-sparing urban areas, characterized by large and non-
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fragmented vegetation patches, could promote sensitive or rare species (i.e. urban

avoiders) with specific feeding or life-history traits. On the other hand, land sharing
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urban areas, with small and fragmented green patches, may favor other traits related

with generalist urban tolerant species or adapters. Additionally, these two urban
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development types seem to differ in predator pressure (Jokimäki et al., 2020),

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potentially affecting the distribution of other traits such as nest type or body size (Møller

et al., 2010). Given that a previous study has identified temporal changes in urban

biodiversity between the wintering and breeding season (Ibáñez-Álamo et al., 2020),

we also predicted seasonal differences in the set of traits associated to urban

development type. This could be explained by the small potential influence of

reproductive parameters (e.g. nesting type) outside the breeding season combined with

changes in the availability of different resources (e.g. food availability or type) between

urban development types depending on the season. We hope that our study will be

useful in identifying and understanding the general mechanisms determining the

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previously observed differences in bird community structures across the urban

landscape.

2. Methods

2.1. Study area and model system

We collected data from avian communities in land-sharing and land-sparing urban

areas in a wide geographical area across Europe. More specifically, we obtained data

from 9 European cities in 6 countries (Fig. 1). We decided to focus on birds because

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they are well-studied in the context of urban ecology (Gil and Brumm, 2014), with

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multiple sources of information about their functional traits (Storchová and Hořák, 2018;

Tobias et al., 2022; Wilman et al., 2014) and because they can be good indicators for
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other taxa (Rodrigues and Brooks, 2007).
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In each city, we selected ten 500 m x 500 m squares, half of them with land-sharing
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development type and the other half with land-sparing development type. We

confirmed this designation with the use of a landscape organization index previously
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published (Ibáñez-Álamo et al., 2020) (see below for more details). Furthermore and

given the relationship between bird biodiversity and the size of green areas (Beninde et
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al., 2015), every single land-sparing square was paired with another land-sharing
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square with similar proportion of green areas to avoid this potential confounding effect,

i.e. there were similar amounts of green space, but they were distributed differently

according to urban development type. Individual study squares within each city were

separated by a mean of 570 (± 65 SD) m from each other, a much longer distance than

the recommended in the literature to ensure their independence (Bibby et al., 1992;

Voříšek et al., 2008). We checked that there were no differences in urbanization

intensity (including urban green areas) through the use of another commonly used

urban index (see Liker et al., 2008 for more details about this index). We found no

significant differences at this respect between urban development types. See Ibáñez-

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Álamo et al., 2020 for additional details in the square selection procedure and

comparisons of urban intensity between urban development types.

2.2. Bird data collection

Within each 500 m x 500 m square, we randomly selected 6-7 point count survey

stations to quantify the bird species present by sight or sound. We used standardized

5-minute point counts with fixed-radius (50 m) carried out within the first four hours of

the day (Bibby et al., 1992) during the breeding season (April - June) of 2016 and the

following wintering season (December 2016 - February 2017). We decided to sample

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these two seasons as they are crucial for birds and could show important bird

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assemblage differences in temperate regions such as those sampled in our study.
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Also, to capture potential changes in bird communities within each season (e.g. early

and late breeders), we carried out two census per season (separated by a month)
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following the standardized method for collecting bird data (Voříšek et al., 2008). We
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used all species detected in both census of the same season for our analyses. All point

counts stations were located at least 100 m apart from each other and from the border
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of the square to minimize the possibility to count the same bird twice and to assure that

birds counted inhabit the sampled square. We used city maps and GPS information
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from each point count to be sure of the use of the same location in all census. Census
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were carried out by different local ornithologists with a long experience performing bird

counting in each study area minimizing potential identification errors. The same

observer carried out all census in their corresponding city.

2.3. Trait collection

We extracted data on species-specific traits from literature (e.g. scientific articles,

books and compilations like Birds of the World; (e.g. Billerman et al., 2020), previously

compiled dataset (e.g. Storchová and Hořák, 2018) and some indices used by other

authors (e.g. Morelli et al., 2019). Following a methodology similar to Sol et al., (2014),

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we extracted data on several traits that could have an effect on the mechanism of

adaptation of species to urbanization.

The selection of these traits included a pool of ecological traits related to habitat

and resource use. These ecological traits are mainly related to specialist species

attributes (e.g. nest specialism, specialism index, foraging specialism) because this

aspect has been previously suggested to vary depending on the urban development

type (Gagné and Fahrig, 2010; Sushinsky et al., 2013). We also collected information

on a set of life-history traits related with reproduction (e.g. clutch size, productivity),

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another aspect associated with urbanization tolerance (Croci et al., 2008). We used

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some of these life-history traits to calculate the position of each species in the so-called

slow-fast life-history continuum (Cauvin et al., 1988), following Sol et al. (2016).
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Previous studies widely use this slow-fast variable due to its potential relationship
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with innovativeness and the adaptability of species to new environments (e.g. (Li et al.,
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2021; Sol et al., 2016, 2014)) and thus could provide interesting information about the

birds’ ability to inhabit in both urban development types. This variable consisted of the
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component 1 obtained from a principal component analysis (PCA) followed by a

varimax rotation, including the following life-history variables for each species:
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fecundity, longevity, age at first breeding, egg mass, length of the incubation period
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and length of the nestling period. The variance proportion explained by the PC1 was

56% for the breeding season and 57% for the wintering season. Before the PCA, the

distribution of each variable was checked graphically and, if necessary, transformed to

obtain more symmetrical distributions, and subsequently centered (around the mean)

and scaled (by the standard deviation) (Tables S2 and S3). Furthermore, we also

collected data on body mass (morphological trait) and breeding system (social trait) as

they have been previously associated with the degree of urban tolerance (Callaghan et

al., 2019; Croci et al., 2008). In total, we extracted data for ecological traits (8

variables), social traits (1 variable), morphological traits (1 variable) and life-history

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traits (5 variables). The definition of all the variables and the data source can be found

in Table S1.

2.4. Statistical analyses

The steps described below have been applied for each set of analyses: breeding (N

= 115 species) and wintering (N = 72 species). The complete list of species for each

season can be found in Table S5. All analyses were performed using R Statistical

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Software version 4.0.3 (R Core Team, 2022).

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To begin with, we started by creating the LSP-LSH index, our designated response

variable, that provides a value of the preference of each species for land-sharing or
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land-sparing urban areas. This LSP-LSH index uses the presence of bird species in
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each landscape development type obtained in our censuses and a previously
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published landscape index (Ibáñez-Álamo et al., 2020) that gives a numerical value

within the land-sparing/sharing continuum to each studied square. To calculate the

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latter landscape index used for the estimation of our response variable, we first divided

each square into 100 cells. We then assessed various landscape characteristics
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providing insights into the arrangement of green spaces and built surfaces within each
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cell (percentage of vegetated cells with built surfaces; percentage of only vegetated

cells) and at the square level (percentage of high vegetation cells –those with >50%

green area– in a single patch; number of green patches; number of vegetated cells).

Finally, we performed a principal component analysis (PCA) using the function prcomp

from the R package ‘stats’ (R Core Team, 2022) and used the first axis (PC1) as the

landscape index (66.8% of total variance explained by this component). Unlike a simple

binary classification into land-sharing or land-sparing categories, this landscape index

offers more detailed information by assigning positive values to land-sharing areas and

negative values to land-sparing areas.

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Subsequently, we employed data separately from the breeding census, which

comprised 115 species, and the wintering period, which included 72 species, to

construct our species-level response variable (the LSP-LSH index) for each season.

These LSP-LSH indices were generated by combining the landscape index value of a

square (Figure 1) with the frequency at which a species was observed in that particular

square. To accomplish this, we first extracted the relevant rows from the original

census data file, retaining only those rows where a species had been observed at least

once. Then, we replicated the landscape index value of a square based on the number

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of times the species was seen in that square. Finally, we combined these values for all

squares for each species and arranged them in ascending order to calculate the

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median. Consequently, the LSP-LSH index represents the median landscape index
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value across all locations where a species was observed, ranging from -4 to 4, and
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thus providing a single value for each species. This value can be interpreted as a

measure of the degree of "landsparingness" or "landsharingness" specific to each

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species in each season, where the minimum and maximum values indicate species
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that are only found in land-sparing or land-sharing urban areas, respectively (see

Figure S1-S2 for a visual representation of the LSP-LSH index).

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In order to determine how species-specific traits associate with the urban

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development type gradient, we first performed a model selection procedure to identify

the relevant predictors that will be later included in phylogenetically-controlled Bayesian

models. For this purpose, we carried out two full linear models (one per season) using

as dependent variable the LSP-LSH index corresponding to each season and, as

independent variables, we included the 15 variables of interest for the breeding season

and 7 variables for the wintering season (see Table S1 for more details). We excluded

breeding-associated traits (7 variables; e.g. nesting type) from the wintering analysis as

this period does not correspond with the reproductive period of any of the studied

species. The only exception was the slow-fast life-history continuum that was kept for

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the wintering analysis because this variable includes breeding (e.g. fecundity) and non-

breeding (e.g. longevity) traits. In addition to these independent variables, our models

included research effort as a control variable, a procedure commonly used in

phylogenetically-corrected analyses (e.g. Ducatez and Lefebvre, 2014; Garamszegi

and Møller, 2010), to control for the available information for each species in the

literature. Research effort is the number of studies per species in Web of Science and

is known to potentially affect some of the variables used in our analyses, such as

longevity (used in the slow-fast continuum) (Møller, 2006; Valcu et al., 2014). The

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models were also weighed by the number of observations per each species used to

calculate the species-specific LSP-LSH index value to control for the effect of the low

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frequency of observations for rare species on the precision of the response variable.
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Additionally, we added taxonomic order as a random effect in these models to control
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for phylogeny (i.e. non-independent evolutionary history of species). We did not include

city as a random effect in these models because of the lack of within-species variation
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(i.e. a single value per species for our response variable). We used linear effects for
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our continuous variables in these models after visually checking for potential linear and

non-linear adjustments of our data. We ran linear models using the lmer function from
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the ‘lme4’ R package (Bates et al., 2015). The weighting for the number of observation

was done by including the variable number of observation in the “weights” argument of
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this function. We used the ‘MuMIn’ R package (Bartoń, 2009) for the selection of the

set of best models applying a selection criteria of Δ AICc ≤ 2 (Δ AICc being the AICc of

the focal model minus the AICc of the best model). This procedure allowed us to select

the relevant variables to use in the following step, which were those that appeared in

the best models set. Before running the saturated models, we checked for

multicollinearity using the vif function from the ‘fmsb’ R package (Nakazawa, 2023). We

found no multicollinearity based on the VIF results for the breeding (VIF = 1.73) or

wintering (VIF = 1.58) models, and thus, no variable initially considered was excluded

from these analyses for this reason. Additionally, we centered (around the mean) and

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scaled (by the standard deviation) all continuous variables to be able to compare the

coefficients from the models outputs due to the different origin and unities of the

variables (Schielzeth, 2010).

The final step of our statistical procedure consisted on using the selected predictors

obtained in the previous step to run phylogenetically-controlled Gaussian linear mixed

models using a Bayesian approximation with the R-package ‘MCMCglmm’ (Hadfield,

2010). The selected variables in the case of the breeding analysis were eleven (based

on 5 models with Δ AICc ≤ 2): foraging substrate specialism, nesting site specialism,

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nesting type, chick developmental type, diet specialism, foraging behaviour specialism,

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habitat specialism, specialism index, annual reproductive investment (i.e. an index

based on egg mass, clutch size and number of broods controlled for body mass - see
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Table S1), breeding attempts per year, and clutch size (see table S4 for additional
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details). For the wintering analysis, the selected variables (based on a single model
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with Δ AICc ≤ 2) were two: habitat specialism and slow-fast continuum. During

exploratory analyses, models were run using alternative priors, including parameter-
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expanded priors, and results were not found to be sensitive to prior specification. The

model used in the final analysis was ran with inverse gamma prior (V=1 and nu=0.02).
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We used a chain for 25 million iterations with burn-in of 1,500,000 and thinning
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intervals of 15,000 iterations that resulted in approximately 1,500 samples from the

posterior distributions for each model parameter. Model convergence was confirmed by

visual examination of trace plots and autocorrelation calculation between iterations.

The phylogenetic signal was then calculated using lambda estimator (λ)(Freckleton et

al., 2002). In order to account for the potential effect that species are not randomly

distributed across the urban landscape but dependent on their common ancestry

(Callaghan et al., 2019; Sol et al., 2014), we controlled the phylogenetic dependency

among species by including phylogeny as a random effect in the model in the form of

the inverse of the ∑ matrix of phylogenetic correlation. We used the phyla-wide

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phylogeny from Jetz et al. (2012), Ericson backbone phylogeny (www.birdtree.org). We

also controlled for the number of observations per species by including the argument

us(sqrt(1/Nobs)):units as an additional random effect (Hadfield, 2019), where Nobs

corresponds with the number of observations per each species used to calculate the

species-specific LSP-LSH index value.

3. Results

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The results from the MCMCglmm analysis for the breeding season showed that

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two species-specific traits were significantly associated with urban development type

(Table 1). These traits were: nesting type open (MCMCglmm: posterior mean = -0.742,
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CI = -1.506 to -0.020, pMCMC = 0.047; Fig. 2) and annual reproductive investment
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(MCMCglmm: posterior mean = -0.438, CI = -0.788 to -0.144, pMCMC = 0.009; Fig. 3).

These results indicate that species that are more often found in land-sparing urban
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habitats during the breeding season have a higher reproductive productivity per year
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than those more common in land-sharing urban areas. Also, they use open nests for

breeding more often than their land-sharing counterparts. Within these traits there was
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one ecological trait (nesting type), and one life-history trait (annual reproductive
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investment).

In contrast, the results for the wintering season showed an effect for the slow-

fast continuum variable (MCMCglmm: posterior mean = -0.393, CI = -0.664 to -0.114,

pMCMC = 0.006). This result indicated that species with a fast way of life (i.e. short

longevity, high fecundity, quickly breeding, with a quick development of the offspring

and small eggs) will be more frequently found in land-sparing urban areas (Fig. 4).

Additionally, we found a marginal significant effect for habitat specialism (MCMCglmm:

posterior mean = 0.197, CI = 0.001 to 0.390, pMCMC = 0.057). This result showed that

species from land-sharing urban areas seem to be more specialized in their habitat

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requirements than those from land-sparing urban areas. Finally, the phylogenetic signal

for the breeding season was lambda posterior mean= 0.343, CI = 0.005 to 0.843, while

for the wintering season lambda mean = 0.373, CI = 0.005 to 0.868.

4. Discussion

The results of our study support the hypothesis that urban development type

(i.e. land-sharing or land-sparing urban areas) selects for a different set of traits in

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birds. Interestingly, this selection seems to differ between the breeding and wintering

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season, which highlights the importance of the seasonal component of this process.

This is in line with the recommendations of considering seasonality when investigating

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effects of urban development type on biodiversity (Ibáñez-Álamo et al., 2020) even
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though urban areas seem to buffer the seasonal composition of bird communities

(Leveau et al., 2021). Our results also match our initial prediction that sensitive species
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(i.e. those with less urban-tolerant traits) are more common in land-sparing than in
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land-sharing urban areas (Gagné and Fahrig, 2010; Suhonen et al., 2022; Sushinsky et

al., 2013). In general, our findings provide an additional understanding about the
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mechanisms behind the observed changes in biodiversity within cities, and particularly
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between land-sharing and land-sparing urban areas (e.g. Ibáñez-Álamo et al. 2020;

Jokimäki et al. 2020).

During the breeding season, urban development type is selecting for nesting

type, an important trait associated with the breeding needs of the species. Our results

indicate that open nesters are more common in land-sparing urban areas, while there

is no relationship between urban development type and closed, cave and cavity

nesters. Breeding in exposed places could be challenging in urban habitats because of

the higher human presence but also due to the presence of cats and dogs that can act

as potential predators (Díaz et al., 2022). For this reason, species using open nests,

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nesting on the ground or close to it, are mainly related with low levels of urban

tolerance (Croci et al., 2008; Kark et al., 2007). In our case, land-sparing areas and its

large and continuous green patches could offer refuge for these open nesters with low

levels of urban tolerance favoring their presence within the city matrix. These results

are in agreement with the higher density of ground nesters (open-cup type) in land-

sparing urban areas compared with land-sharing ones and could be due to a higher

nest predation pressure in the later (Jokimäki et al., 2020). Then, our results could be

explained by differential survival (higher in land-sparing) or specific-habitat selection

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processes against urban areas showing a higher density of potential predators

(Suhonen et al., 1994). Even if potential nest predators or their abundance do not differ

between urban development types

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(Jokimäki et al., 2020), non-lethal
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activities/behaviors (e.g. being more conspicuous in land-sharing areas) could have a
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strong influence at the population level (Cresswell, 2008; Díaz et al., 2022) ultimately

determining the decision of birds to breed in certain urban areas. Interestingly, species
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using other nest types did not show any significant difference between urban
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development types probably due to the fact that they suffer less from nest predators as

their nest are more protected (Fontaine et al., 2007). These results are in contrast to
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another study that found lower proportion of cavity nesters in residential areas

compared to parks (LaMontagne et al., 2015). However, this study was conducted in a
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single city and the building characteristics of residential areas may not favor cavity

species in that particular case.

In addition to these ecological traits, we found that some life-history traits could

also be important in this context. Bird species that are more often detected in land-

sparing urban areas have also a higher reproductive investment than those from land-

sharing areas. Previous studies suggest that the reduction in productivity per nesting

attempt is related with the lack of natural food and its low quality in urban areas

(Chamberlain et al., 2009; Seress et al., 2020). Furthermore, the presence of native

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vegetation (more typical from land-sparing urban areas, that can include native forest

remnants) is also related with higher food availability (Collas et al., 2017; Zanette et al.,

2000). Thus, food availability/quality could be indirectly driving the observed differences

in annual reproductive investment between urban development types. Another possible

explanation could be that land-sharing areas have a higher presence of bird feeders

(Fuller et al., 2008; Ibáñez-Álamo et al., 2020). Although bird feeders can be important

for the survival of birds (Jokimäki & Kaisanlahti-Jokimäki 2012; Lahti et al., 1998), they

may also have negative consequences on avian reproduction because they could be

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related to an increase in nest predation (Broughton et al., 2021; Hanmer et al., 2017) or

could even increase adult mortality due to the transmission of diseases or parasites

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between individuals (Chamberlain et al., 2009; Moyers et al., 2018). However, the
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influence of bird feeders should be taken with caution given the important variation in
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its use among cities (Reynolds et al., 2017) and the latitudinal variation in their potential

benefits for winter survival (more important in higher latitudes). In fact, this city-level
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variation applies to many factors beyond bird feeders (e.g. proportion of native
na

vegetation, artificial light or noise pollution) and, thus, future studies directly exploring

the differences in natural and anthropogenic food availability/quality (or other factors)
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between land-sharing and land-sparing urban areas will be particularly interesting at

this respect.
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Our findings for the wintering season showed that species more often found in

land-sharing urban areas have a slower pace-of-life strategy compared with those from

land-sparing urban areas. This result implies that typical land-sharing bird species

should be those with low reproductive effort and long lifespan (e.g. Larus argentatus;

Fig. S2). Longevity has been positively associated with innovativeness (Sol et al.,

2016). Thus, we could speculate that long-lived species can be better at dealing with

the closer human-contact and more complex landscape organization of land-sharing

urban areas (e.g. with more fragmented green areas). In contrast, species less prone

16
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to innovate would find refuge in the more homogeneous and less disturbed large green

areas (e.g. parks) of land-sparing urban areas. This would initially contrast with the

general finding that fast-lived species are more prone to take risks (another component

of the pace-of-life syndrome), but this association disappears in urbanized

environments (Sol et al., 2018), thus fitting this potential explanation. Our finding for the

wintering season showing that land-sparing bird species follow a faster pace-of-life

strategy matches our previously discussed finding that species with higher annual

reproductive investment are associated with land-sparing urban areas during the

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breeding season. However, the slow-fast continuum variable was not even selected as

an important predictor for the breeding season, which could suggest that non-

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reproductive traits (e.g. longevity) are more important outside the breeding period, just
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as we initially expected.
re
In addition, we found a trend indicating that species more often seen in land-
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sparing urban areas could be more habitat generalists. This result contrasts with our

prediction that typical land-sparing birds would be more specialized (Gagné and Fahrig,
na

2010; Sushinsky et al., 2013). This finding is difficult to explain, however it could reflect

that species preferring large green patches from land-sparing urban areas could have
ur

wider habitat preferences for natural environments but a low preference for heavily-
Jo

influenced human landscapes. One potential example for this could be the meadow

pipit (Anthus pratensis), a species only found in land-sparing areas during winter, that

can be found in a wide variety of natural open habitats like tundra, moorland, bogs,

saltmarshes, mountain meadows but only occasionally in human-influenced areas such

as arable land (Tyler and Sharpe, 2020).

Our results for bird traits in winter were initially surprising given that land-

sharing urban areas in Europe showed higher functional diversity compared with land-

sparing areas (Ibáñez-Álamo et al., 2020). One possible explanation could be that

differences in functional diversity are based on other traits than those used in our study

17
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(e.g. susceptibility to human disturbance). More studies are clearly needed to

disentangle these contrasting findings and to better comprehend the seasonal variation

of traits distribution within the urban matrix.

Previous studies have detected that urban tolerance is phylogenetically

restricted (Callaghan et al., 2019; Sol et al., 2014; Winchell et al., 2020; but see Evans

et al. 2011). However, we found weak values (0.34 and 0.39 for breeding and winter,

respectively) of phylogenetic signal in our analyses indicating the lack of specific bird

evolutionary lineages more prone to be found in a specific urban development type.

of
5. Conclusions
ro
-p
We provide evidence that urban development type is filtering species-specific
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traits probably inducing changes in urban community assembly. This process could be
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associated with the characteristics of green patches in land-sharing and land-sparing

urban areas (e.g. fragmentation). Fragmentation of urban greenspace can induce the
na

same negative effects as in other landscapes and some studies have recommended

improving urban corridors, habitat diversity and resource availability as a way to

ur

enhance urban biodiversity (Beninde et al., 2015; Fernández-Juricic and Jokimäki,

Jo

2001). Our findings thus provide important information regarding the possible

management actions to improve bird communities in different urban areas. Our study

did not consider possible differences in noise and artificial light pollution levels, and

their possible impacts on birds between urban development types. Further studies are

needed to disentangle the potential effects of green site characteristics as well as

pollution at the community level. Our results show that land-sparing urban areas

promote bird species with higher annual reproductive investment and using open nests

during the breeding season, and fast-lived species during the winter. These results are

in line with other previous studies showing that urban avoiders are more common in

18
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land-sparing urban areas (Gagné and Fahrig, 2010; Suhonen et al., 2022; Sushinsky et

al., 2013). Our findings also highlight the importance of integrating a seasonal

component in this kind of urban ecology studies. Future studies should try to identify

the generality of our findings in other urban contexts (e.g. tropical areas, global south

cities) and explore the variation in species-specific traits associated with the local

variation of urban attributes or citizen practices. Overall, our findings could be useful for

city planners willing to design cities that can retain a higher number of bird species.

This is particularly important not only from the ecological point of view (e.g. favoring

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ecosystem functioning; (Gonzalez et al., 2020), but also for improving the citizen’s

wellbeing (Methorst et al., 2021).

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Acknowledgements
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We would like to thank Olivia Sanllorente for her constant support and stimulating
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discussions on the project. We are very grateful to Dan Chamberlain and another
na

anonymous reviewer whose suggestions have considerably improved our study. This

study has been funded by the Spanish Ministry of Science and Innovation (PID2019-
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107423GA-I00 / SRA (State Research Agency / 10.13039/501100011033).

Jo

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Legends

Figure 1. European map of the locations of the 9 cities and the bird census

design. On the right part, there are two study squares representing the

extremes of the urban landscape gradient (LSP corresponds with land-sparing

and LSH with land-sharing urban areas) and the continuous nature of this

gradient represented by different colors.

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Figure 2. Estimates and 95% CI of the response variable (LSP-LSH index) for

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the different nesting types (cave, cavity, close and open-cup) for the breeding
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season. Sample size: 115 species. Negative values of the response variable
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indicate species more often found in land-sparing urban areas (in blue) while

species more common in land-sharing urban areas are represented with

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positive values (in red).

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Figure 3. Relationship between the response variable (LSP-LSH index) and the
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productivity (log-transformed) of each bird species during the breeding season.

Sample size: 115 species. Regression line and standard error are marked in

grey. Negative values of the response variable indicate species more often

found in land-sparing urban areas (in blue) while species more common in land-

sharing urban areas are represented with positive values (in red).

Figure 4. Relationship between the response variable (LSP-LSH index) and the

slow-fast life-history continuum variable for the wintering season. Sample size:

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72 species. Regression line and standard error are marked in grey. Negative

values of the response variable indicate species more often found in land-

sparing urban areas (in blue) while species more common in land-sharing urban

areas are represented with positive values (in red).

Table 1. Results of the final Bayesian phylogenetic analysis for the breeding

season (MCMCglmm). Sample size: 115 species. Results statistically significant

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(pMCMC ≤ 0.05) are in bold. Colors of the name of the variable indicate the

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type of trait: ecological traits are marked in green and life-history traits in blue.
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Table 2. Results of the final Bayesian phylogenetic analysis for the wintering
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season (MCMCglmm). Sample size: 72 species. Results statistically significant

(pMCMC ≤ 0.05) are in bold. Result marginally significant (pMCMC = 0.05-0.08)

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are marked with “*”. Colors of the name of the variable indicate the type of trait:

ecological traits are marked in green, social traits in grey, morphological traits in
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red and life-history traits in blue.

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Figure 1.

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Figure 2.

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Figure 3.

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Figure 4.

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Table 1.

Post. Lower 95% Upper 95%

pMCMC
mean CI CI
Fixed Effects

Nesting type (open) -0.742 -1.506 -0.020 0.047

Nesting type (cavity) -0.246 -1.109 0.496 0.534

Nesting type (closed) -0.437 -1.317 0.425 0.310

Chick Developmental Type

-0.025 -1.184 0.943 0.902

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(precocial)

Chick Developmental Type (semi-

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-0.291 -1.111 0.564 0.481
altricial) -p
Chick Developmental Type (semi-
0.170 -0.837 1.377 0.786
precocial)
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Foraging substrate specialism -0.354 -1.048 0.313 0.314
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Nesting site specialism -0.477 -1.160 0.298 0.208

Diet Specialism -0.104 -1.005 0.707 0.837

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Foraging behaviour specialism -0.176 -0.990 0.536 0.655

Habitat specialism -0.162 -0.976 0.550 0.694

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Specialism index 0.840 -1.516 3.052 0.466

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Annual reproductive investment -0.438 -0.788 -0.144 0.009

Breeding attempts per year 0.228 -0.049 0.478 0.102

Median clutch size 0.061 -0.216 0.311 0.639

Research effort 0.106 -0.069 0.310 0.290

Random Effect

Phylogeny 0.012 0.003 0.678

Number of observations 1.718 0.005 3.212

Phylogenetic signal (ʎ) 0.343 0.005 0.843

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Table 2.

Post. mean Lower 95% CI Upper 95% CI pMCMC

Fixed Effects

Habitat Specialism 0.197 0.001 0.390 0.057*

Slow-Fast Continuum -0.393 -0.664 -0.114 0.006

Research effort 0.227 0.044 0.424 0.023

Random Effects

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Phylogeny 0.011 0.002 0.527

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Number of observations 2.869 0.035 6.806

Phylogenetic signal (ʎ) 0.373

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0.005 0.868
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Urban landscape organization is associated with species-

specific traits in European birds.

Highlights

• Avian traits are different depending on urban landscape organization.

• Bird species living in land-sparing urban areas are more specialists.
• Lower annual reproductive investment is more common in land-sharing areas.
• Land-sparing urban areas filter for fast-lived species in winter.

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