ORIGINAL ARTICLE

Bogumiła Maciusik • Magdalena Lenda

Piotr Skorka

Corridors, local food resources, and climatic conditions affectthe utilization of the urban environment by the Black-headedGull Larus ridibundus in winter

Received: 16 April 2009 / Accepted: 14 September 2009 / Published online: 20 October 2009� The Ecological Society of Japan 2009

Abstract Black-headed Gulls Larus ridibundus (BHGs) inurban areas are a public nuisance. The aim of this study isto investigate the factors affecting the occurrence andabundance of the BHG foraging in urban areas in winter.The study was conducted in the city of Krakow (southernPoland) in four easily identifiable urban habitats: (1)areas with blocks of flats, (2) areas with congested hous-ing, (3) detached single-family housing and (4) greenareas. In each of these four habitats, 60 small (1-ha) plotswere randomly chosen, and the bird’s presence andabundance were noted. Results revealed that birds oc-curredmost frequently and in the largest numbers in plotswith blocks of flats and green areas as well as plots locatedclose to rivers and water reservoirs. This highlights theimportance of ecological corridors and stepping-stonesfor the presence of this species in the city. Food resourceshad no effect on the presence of the gulls but the abun-dance of the species was positively correlated with thenumber of litter-bins. This indicates that local food re-sources could be more important than large landfills forthis species in urban habitats during winter. No humandisturbance indices had an effect on the occurrence andabundance of the BHG. Higher temperature and lack ofsnow cover positively affected utilization of the urbanhabitats by the species that indicates that global warmingmay speed up synurbanization of the BHG. To controlthe number of BHGs in urban areas, we suggest pre-

venting access to local food resources by placing litterbins with waste baskets that are inaccessible to animals.Also, the public should behave appropriately towardsgulls and refrain from feeding them intentionally.

Keywords Movement Æ Foraging Æ Landscape ÆUrban ecology Æ Global warming

Introduction

There are many factors that lead to cities being colonizedby animals. The urban environment offers the opportu-nity to find food with lower costs than are normally spentby individuals in their natural habitat (Chace and Walsh2006). Contrary to public perception, rich resourcesof food are numerous in cities. They are primarily sour-ces that are associated with the city’s main resident—humans. Leftover food discarded in tips or food stored inwarehouses or pantries are easily accessible sources offood for birds (Luniak 2004; Kelcey and Rheinwald2005). In addition, food is readily available in birdfeeders, or deliberately left out in green areas, parks, orbeside urban sections of rivers (Jones and Reynolds 2008;Walasz 2000; Avilova and Eremkin 2001; Jerzak 2001).Another place that is very attractive in respect to theavailability of food are suburban landfills, where flocksof different bird species forage; mostly corvids and birdsof prey (Elliott et al. 2006).

Cities are characterized by amilder climate with higheraverage annual temperatures (Luniak 2004). This, there-fore, represents a particularly attractive place for variousspecies to survive the critical period of the year, which isthe winter (Chace andWalsh 2006). It has been noted, forinstance, that urban populations of birds are more settledand nest more often within the breeding season thanpopulations living outside cities (Luniak 2004).

However, the city also brings some threats to birdpopulations. One of them is humans. It was found thatwhile foraging in the city, birds are often disturbed by

Electronic supplementary material The online version of this article(doi:10.1007/s11284-009-0649-7) contains supplementary material,which is available to authorized users.

B. Maciusik Æ M. LendaInstitute of Environmental Sciences,Jagiellonian University, Gronostajowa 7,30-387 Krakow, Poland

P. Skorka (&)Institute of Nature Conservation,Polish Academy of Sciences,Mickiewicza 33, 31-120 Krakow, PolandE-mail: skorka@iop.krakow.pl

Ecol Res (2010) 25: 263–272DOI 10.1007/s11284-009-0649-7

passers-by, or dogs accompanying them (Randler 2003;Chace and Walsh 2006). Large human disturbance maycause the birds to avoid places where the presence ofhumans is frequent (Fernandez-Juricic and Jokimaki2001). It was also found that frequent disturbance couldbe an important factor in selection, and in effect, causeschanges of behavior and certain morphological charac-teristics of urban animal populations (Cooke 1980;Ditchkoff et al. 2006). Cars are also a threat to birdsliving in urban areas, which cause damage and death tobirds (Erritzoe et al. 2003; Ditchkoff et al. 2006). An-other factor in the increased mortality of urban birdpopulations is collisions with buildings (Klem 1990).High office buildings, covered with glass, reflect the skyand remain unseen by birds. The same phenomenontakes place at noise-protective screens along busy roads(Chace and Walsh 2006). Therefore, the animal responseto positive and negative factors affects its occurrence inurban landscape.

The occurrence of animals in the urban environmentmay be also linked to the characteristics of habitats atthe landscape scale (Chace and Walsh 2006). Manyanimals’ habitats or resources in urban areas are smallpatches isolated from each other (Fernandez-Juricic andJokimaki 2001). Therefore, the occurrence of animals insuch habitat patches depends upon their capacity tocolonize such habitat patches as well as the patch sizeand isolation. An important element in enabling themovement of animals, utilization, and the colonizationof urban environment may be the ecological corridorsand stepping-stones (Fernandez-Juricic and Jokimaki2001; Manson et al. 2006, 2007). Corridors and step-ping-stones are strings or patches of habitats that pro-vide food and shelter while animals disperse, migrate, orforage. It would seem that birds do not need ecologicalcorridors because of their high mobility. However, theresults of different research show that the movements ofbirds may be significantly disturbed by the existence ofbarriers (Hodgson et al. 2007; Skorka et al. 2009). Theexistence of ecological corridors and stepping-stonesmay, therefore, facilitate the intermingling of differentspecies in urban areas and their utilization and/or col-onization.

The occurrence and/or use of the urban environmentprobably depend on the locations in which individualsaccumulate. Such places may be pools of individualscolonizing the urban environment (see also the conceptof ‘‘source–sink’’ Pulliam 1988). These ‘‘sources’’ ofindividuals may be large fragments of natural habitats,for example: meadows, forests, and rivers as in the caseof wintering waterbirds (Ockinger and Smith 2007;Shwartz et al. 2008). This hypothesis, however, has notyet been tested in the case of the urban environment.

Among birds, gulls are a group of species that fre-quently occur in the urban environment. Due to theirclamorous behavior, the possible transmission of dis-eases and griming by excrements and even aggressiontowards people they are a serious problem in many citiesover the world (Rock 2005; Calladine et al. 2006). They

also incur substantial economic costs for humans be-cause they necessitate the implementation of varioustechniques to control their number as well as the re-moval of the effects of their behavior (which mostly in-volves cleaning the sites visited by gulls; Belant 1997;Belant et al. 1998; Rock 2005). Therefore, understandingwhich factors affect occurrence and abundance of suchspecies in the urban environment are of primary con-cern.

The purpose of this study was to describe the factorsaffecting the presence and abundance of the Black-headed Gull Larus ridibundus (BHG) in the urbanenvironment, in winter. We investigated which factors,linked with (micro)habitat and landscape features, affectthe utilization of a variety of urban habitats by thestudied birds. In particular, we tested the followingpredictions: (1) the presence of BHGs and their abun-dance should positively depend on the availability offood sources (the number of litter-bins, proximity ofrefuse tip) and the presence of ecological corridors andstepping-stones (proximity of watercourses and waterreservoirs, respectively), (2) the presence and the abun-dance of BHGs should negatively depend on humandisturbance (the number of people, the distance tostreets with heavy traffic), (3) the presence and abun-dance of BHGs should depend on the proximity of‘‘sources’’ of individuals (the urban section of a largeriver—the Vistula River).

Weather often varies during the winter, therefore, wewere also interested in the manner the climatic condi-tions during the winter do affect presence and abun-dance of the species in urban habitats.

Materials and methods

The study species

The BHG is a medium-sized waterbird from the Laridaefamily (Supplementary material). Individuals of bothsexes are similar in plumage. During the breeding sea-son, in May, the feathers on the head are dark-brown.Until they are 2 years old, juvenile individuals feature abrown upper body, and at the tail end a distinguishablebrown stripe. The length of the body ranges from 38 to40 cm, the wing-span measures approximately 95 cmand it weighs from 260 to 350 g (Snow and Perrins1998).

BHG occurs throughout Poland in winter. Its pres-ence is strongly associated with river valleys, rivers, andlakes. In southern Poland, its main gathering site inwinter is in the city of Krakow, mostly along the banksof the Vistula River, which flows through the city center(Walasz 2000). The number of individuals estimatedthere is nearly 2000 (Walasz 2000). The Vistula River ismajor roost site for BHGs in Krakow.

The presence of BHGs in large numbers in the citycauses real conflicts between the birds and humans. Thegulls are often aggressive towards people and their pets.

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Gulls’ droppings make many urban areas dirty and thisheightens public anxiety over the possible transfer ofdiseases (mostly in the form of bird flu). This problembecomes more important as gulls often appear at pondsthat serve as drinking-water reservoirs for the city’sinhabitants. A large number of birds may also pose aproblem for the city’s international airport.

Study area

Krakow lies in an area of several geographical regions: theGate of Krakow, Sandomierz Dale, Oswiecim Dale, andWest-Beskidy foothills. The main area of the city islocated in the Vistula River valley. The river networkforms the River Vistula and its numerous tributaries: theWilga, Rudawa, Białucha, Dłubnia, Sanka, and others(Fig. 1).

The city covers an area of 327 km2, with 756000inhabitants (an average density of 2314 people/1 km2;Anonymous 2007). The main location for winteringwaterbirds is along the section of the Vistula River thatpasses through the city center (Fig. 1). The averagetemperature in winter (January) is �2.8�C, precipitationis 650–700 mm, and snow cover is 15 cm on average andlies about 60 days (Matuszko 2007). There is a constanttrend of occurrence of mild winters in recent years(Matuszko 2007).

Surveys for BHGs in urban environments

To determine the factors affecting the presence ofthe BHG in the city, random samples of 1-ha plots inthe following four major urban habitats were chosen:(1) congested urban buildings, (2) blocks of flats, (3)districts of detached, single-family houses, and (4) greenareas (see: Supplementary material). The plots were

established by generating random coordinates. Thesampled coordinate was the upper left side of the topsquare of 100 · 100 m. The plot could not overlap. Ineach habitat type, there were 60 plots. In total, therewere 240 1-ha plots. Areas of congested housing were allresidential buildings (usually with 3–5 floors) locatedclose to each other, often forming a system of buildingsadjacent to each other, sometimes containing smallgardens. An example of this habitat is the city’s old townand its neighboring areas, and also buildings in thevicinity of Central Square in the Nowa Huta district.The blocks of flats studied were generally newer build-ings than those found in congested urban developments,the buildings were usually free-standing and higher (6–14 floors). Single-family districts were characterizedpredominantly by numerous detached houses with smallgardens. Garden trees were numerous in this habitat.The final habitat, green areas, was defined as all theparks, squares, meadows, and fields located in theadministrative limits of the city, adjacent to buildings, orwithin residential areas.

Each small plot was observed five times between thebeginning of November 2006 and the end of February2007. Each plot survey lasted 10 min in favorableweather conditions (without snow or rain). The numberof foraging gulls was noted. We noted the maximumnumber of birds present in a plot during a 10-minobservation period. All birds were easily visible becausethe study plots were relatively small (1 ha) and the ob-server moved within them to cover the entire area byvisual observation. During each survey, the presence ofsnow cover (noted as binary variable: 0––no snow cover,1––presence of snow cover) and temperature were noted.Snow cover was recorded as present (1) if at least 90% ofa plot area was covered with snow. Usually, it was veryeasy to determine if snow cover was present or not. Thesnow cover, if present, was usually thick. Therefore, itwas straightforward to note its presence/absence. Thetemperature was noted in each plot during each surveyusing a BAMR AZ 8706 electronic thermometer.

In each survey, the number of people outside as wellas the number of free-standing litter-bins and refuseheaps, were noted. Surveys were done between 0800 and1300. Surveys were conducted in a random manner,however the random sampling was stratified to appro-priately cover the total sampling period in each plot, toexclude possible differences in bird activity during theday. Binoculars of 8 · 10 and 10 · 50 were used duringobservations.

The following landscape variables describing 1-haplots were taken from aerial photographs digitalized inArcGIS (ESRI Institute, Redlands, CA, USA) software:(1) distance (m) to the city section of the Vistula River,which is a major wintering place for BHGs in Krakow,(2) distance (m) to the nearest watercourse (including theentire length of the Vistula River within the city’sadministrative borders), (3) distance (m) to the nearestwater reservoir, (4) distance (m) to the urban landfill sitein Krakow-Barycz, (5) distance (m) to the nearest urban

Fig. 1 Map of the study area of Krakow city. The filled circlesindicate the section of the Vistula River that flows through the citycenter

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arteries, as defined in this study as a street with at leastfour lanes.

The number of litter-bins and refuse heaps within theplot and distance to urban landfill sites were variablesdescribing the availability of food for BHGs. The dis-tances to the nearest watercourse and water reservoirwere variables that describe the habitat which enhancesmovements in urban areas, and thus illustrate the pres-ence of ecological corridors and stepping-stones,respectively. In addition, the distance to the urban sec-tion of the Vistula River was also declared a variablethat describes the distance from the ‘‘pool of individu-als’’, which could enter the urban habitat. The numberof people present within the plot and distance to theurban arteries were the variables that potentially nega-tively affected the presence and abundance of birds(disturbance, collisions with vehicles).

Statistical analysis

In order to determine which factors affect the presenceof BHGs in the study plots, a generalized linear modelwith logit link-function was used. The dependent vari-able was the presence or absence of the gulls within thestudy plot (coded as 1 or 0, respectively). The study plotwas labeled ‘‘presence of BHGs’’ when at least oneindividual was noted at least once out of five observa-tions made in the plot. The independent environmentalvariables in this analysis were: type of urban habitat,number of litter baskets within the plot, distance tourban landfill, distance to the nearest watercourse,distance to the nearest water reservoir, distance to theVistula river, average number of people present withinthe study plot, and distance to the city’s major arteries.We also incorporated geographic coordinates (geo-graphical longitude and geographical latitude) into themodel. To make the analysis more flexible, we alsoallowed for non-linear effects by introducing a centered-squared-term of the variables ‘‘longitude’’ and ‘‘lati-tude’’. In the first step, all interactions between thehabitat type and continuous environmental variableswere included in the model. The insignificant interac-tions were removed from the model. The final modelcontained all simple effects and significant interactionterms.

To determine which factors affect the abundance ofBHGs within the study plots, a general linear model wasused. The dependent variable was the average number ofbirds noted during five checks within the study plots.Independent variables were the same as in the case oflogistic regression analysis. In this paper, both thepresence and abundance should be understood as habi-tat use rather than the presence of a ‘‘local population’’within the plot, as birds were mobile. The model build-ing procedure was as described above.

To analyze how climatic factors (temperature andpresence of snow cover) affect presence and abundanceof BHG within the study plots we used generalized linear

mixed model with logit and identity link functions,respectively. We used identity link instead of log link inthe analyses of abundance, because in our study the dataon bird abundance fitted the normal distribution muchbetter than the Poisson distribution, which is often usedto model count data. The independent variables weretemperature (continuous variable), and presence of snowcover (binary variable: 0––no snow cover, 1––presenceof snow cover). We built the models separately for snowcover and temperature. Moreover, each model containedthe following independent variables: date of the census,habitat type, and geographic coordinates. We includedthe date of census (number of days from November 1) totest the effects of temporal variation in abundance ofbirds. Because the date may influence the number ofgulls in a non-linear way, we also included a centered-squared-term of the variable ‘‘date’’ to allow modelingof this effect. To make the analysis more flexible, we alsoallowed for non-linear effects by introducing a centered-squared-term of the variables ‘‘longitude’’ and ‘‘lati-tude’’ and interaction term between these variables andclimatic conditions (snow cover and temperature). Forexample, if birds move outside the city center duringwarmer periods we should expect non-linear effects of‘‘longitude’’ and ‘‘latitude’’ to interact with temperature:birds should be more abundant in the plots located morenorth and south as well more west and east from the citycenter during warmer periods. On colder days, birdsshould be more gathered near the city center. Finally, wealso introduced additional terms in the statistical modelsdescribing effects of climatic conditions: interaction be-tween ‘‘longitude centered-squared (or latitude centered-squared) ‘‘*’’ temperature (or snow cover) ‘‘*’’ habitattype’’, to find out if presence of birds and their abun-dance is differentially affected by climatic conditions invarious urban habitats after accounting for geographicalposition of the study plots.

In every model for climatic conditions, ID of thestudy plot was included as a random factor. Thus, thesample size in this analysis was enlarged becausethe surveys were replicated five times in every plot (240plots · 5 surveys = 1200 possible data points). Allgeneral and generalized linear models were analyzed inSAS 9.1.

Spatial autocorrelation among plots was tested bycomparing mean abundance of birds and geographicalcoordinates of each plot with Mantel test (Fortin andGurevitch 1993; Legendre 1993; Koenig and Knops1998). Mantel test evaluates the similarity between anecological distance matrix and a geometric distancematrix. If spatial autocorrelation exists, then the closerthe plots are in geometric space, the more similar thevalues of the abundance in the plots should be. We usedMonte Carlo simulations to test the hypothesis thatthere was no correlation between bird abundance andgeographical coordinate matrix: P-values were based onthe proportion of 9999 Monte Carlo simulations.Mantel test was performed using PC-ORD (McCuneand Mefford 1999).

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Results

Factors affecting the presence and abundance of BHGsin the urban environment

The probability of the presence of BHGs within the studyplots depended on the type of habitat, and it was highest inblocks of flats and green areas (Table 1, Fig. 2a). Theprobability of the presence of birds was also significantlyhigher within the study plots in the vicinity of watercourses,water reservoirsandtheVistulaRiver (Table 1,Fig. 2b, c,d).

For the plots where BHGs were observed at leastonce, the average number of birds was dependent on thehabitat type, with the largest numbers recorded at theblocks of flats (Table 2, Fig. 3a). The abundance was

also positively linked to the number of litter-bins withinthe study plots (Table 2, Fig. 3b) but was negativelylinked with distance to the watercourse (Table 2,Fig. 3c). The number of birds seemed to be negativelydependent on distance to the Vistula River, but therelationship was marginally insignificant (Table 2).

No interaction between habitat type and explanatoryvariables was significant in models for presence andabundance of birds within study plots, therefore theinteraction terms were removed from the final modelcontaining only simple effects.

We found no spatial autocorrelation (Mantel test,r = 0.06, P = 0.09) among abundance of birds in clo-ser plots. We also checked for correlations amongexplanatory variables (Table 3). We found six significant

Table 1 Factors affecting thepresence of Black-headed Gullsin the urban environment

Results of the generalized linearmodel with logit-link function.Variance explained by themodel R2 = 64% (N = 2401-ha study plots)aReference category of the var-iable ‘‘habitat’’ (see Kleinbaumet al. 1997; Kutner et al. 2004)

Effect Estimate (SE) df v2 P

Habitat – 3 20.689 0.001Blocks of flats 1.6713 (0.5128) – – –Green areas 1.2197 (0.4948) – – –Congested urban buildings �1.1171 (0.4654) – – –Single-family houses 0a – – –Number of litter-bins 0.2146 (0.1558) 1 1.489 0.222Distance to landfill 0.0013 (0.0010) 1 1.991 0.158Distance to nearest watercourse �0.0066 (0.0011) 1 117.593 <0.001Distance to nearest water reservoir �0.0006 (0.0002) 1 6.139 0.013Distance to the Vistula River �0.0007 (0.0002) 1 10.903 0.001Average number of people �0.0063 (0.0380) 1 0.094 0.759Distance to major arteries 0.0004 (0.0004) 1 1.193 0.275Longitude �0.3536 (0.3666) 1 2.416 0.120Latitude �0.0593 (0.0390) 1 0.935 0.334Longitude ^2 0.0344 (0.0355) 1 1.915 0.166Latitude ^2 0.0507 (0.3720) 1 0.959 0.327

Fig. 2 Factors affecting thepresence of foraging Black-headed Gulls in the urbanenvironment in winter.a Proportion of the plots in agiven habitat where gulls werenoted at least once. b Mean(with 95% confidence intervals)distance to nearest watercourse.c Mean distance to nearestwater reservoir. d Meandistance to the city section ofthe Vistula River from plotswhere gulls were observed (1)and not observed (0)

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correlations (Table 3) but the values of the correlationcoefficient were low (all r below 0.300).

Effect of climatic conditions on utilization of urbanenvironment by BHGs

We found that presence of BHGs within the landscapeplots was positively related with the temperature (gen-eralized linear mixed model with logit link function;slope ± SE = 0.026 ± 0.005, F1, 1171.1 = 16.942, P <0.001, partial R2 = 21%, Fig. 4a) but not with the pres-ence of snow cover (generalized linear mixed modelwith logit link function; slope ± SE = �0.035 ± 0.049,F1, 1080.1 = 1.281, P = 0.258, n.s., partial R2 = 3%).However, the number of birds within the plots was posi-tively related to temperature (general linear mixed model:F1, 357.2 = 27.701, P < 0.001, partial R2 = 17%, Fig. 4b) and the absence of snow cover (general linear mixedmodel: F1, 242.5 = 10.867, P < 0.001, partial R2 = 13%,Fig. 4c). We also found that the date in the seasonaffected the number of gulls in a non-linear way (generallinear mixed model: slope ± SE = �0.122 ± 0.059,F1, 248.5 = 4.040,P = 0.045, partialR2 = 11%,Fig. 4d).Their numbers were the highest in themiddle of the winter.Interestingly, there was no correlation between the tem-perature and date of the census in the study (r = 0.150).Also, no significant correlation was found between thetemperature and the squared-centered term of the date ofthe census (r = �0.097). None interaction was significantwhat indicates that the effects of climatic conditions on thebirds’ presence and abundance were independent on hab-itat type and geographic position of the plots in the city.

Discussion

Factors affecting the presence and abundance of BHGsin the urban environment

The urban areas where BHGs occurred most frequently(and in the highest number) were blocks of flats and also

green areas. In other habitats, BHGs occurred much lessfrequently and in smaller numbers (Figs. 2a, 3a). Itseems that these differences may be associated with ac-cess to food and the ability of movement in such habi-tats. Within the areas with blocks of flat, the buildingswere often built separately from each other with vastareas (mostly grass lawns) where the birds have betteraccess and may forage during warmer periods.

Our results show that a key factor, positively relatedto the presence of BHGs within the city during thewinter, is the different types of ecological corridors andstepping-stones. The corridors for this species are vari-ous types of watercourses and the stepping-stones arereservoirs of standing water, which result from the factthat BHGs are closely associated with water-basedenvironments. Birds moving along streams and waterreservoirs have the opportunity of foraging and restingsafely. It is also probable that in this way the gulls gaininformation about potential breeding habitats, whichhas been observed in other species (Thomson et al. 2003;Arlt and Part 2008). The importance of ecological cor-ridors in the dispersion of animals in the urban envi-ronment has also been highlighted in other works(Fernandez-Juricic 2000). Further studies should focuson the management of such corridors and stepping-stones in order to improve their quality and their pos-sible use by other species of waterbirds (Manson et al.2006).

Admittedly, in our study, the terms ‘‘ecological cor-ridors’’ and ‘‘stepping-stones’’ seem to have a slightlydifferent meaning than the usual definition saying thatthese are an environments promoting connectivityamong habitats patches and are different from ordinaryhabitat in the sense that a corridor or stepping-stoneitself does not work as a habitat. Moreover, water res-ervoirs and small watercourses could be a source habitatfor BHGs, but we do not believe this is the case in ourstudy. BHGs mostly fly along small watercourses andrarely forage there. The number of gulls in watercoursesvaries considerably (unpublished data), which indicatesthat the gulls do not use small watercourses constantly.The situation is different on the Vistula River, where

Table 2 Factors affecting thenumbers of Black-headed Gullsin the urban environment

General linear model results;adjusted R2 = 68% (N = 991-ha study plots). For explana-tion, see Table 1

Effect Estimate (SE) df F-value P-value

Habitat – 3 21.575 <0.001Blocks of flats 0.5786 (0.1044) – – –Green areas 0.7380 (0.1146) – – –Congested urban buildings �0.5256 (0.1466) – – –Single-family houses 0* – – –Number of litter-bins 0.1236 (0.0382) 1 10.473 0.002Distance to landfill 0.0001 (0.0001) 1 0.022 0.881Distance to nearest watercourse �0.0026 (0.0002) 1 120.384 <0.001Distance to nearest water reservoir �0.0008 (0.0006) 1 2.198 0.142Distance to the Vistula River �0.0007 (0.0003) 1 3.383 0.065Average number of people 0.0151 (0.0090) 1 2.767 0.100Distance to major arteries 0.0004 (0.0081) 1 0.547 0.461Longitude �0.0027 (0.0095) 1 0.077 0.781Latitude �0.0121 (0.0101) 1 1.424 0.236Longitude ^2 0.0055 (0.0078) 1 0.351 0.555Latitude ^2 0.0012 (0.0025) 1 1.685 0.198

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BHGs are present in large numbers, stay there andforage. Similarly to small watercourses, water reservoirsare the sites where BHGs never gather for longer periodsin winter. They usually move between the reservoirsand search the surrounding areas for food resources.Furthermore, water reservoirs are frozen for most ofthe winter, even during warmer days, therefore they donot provide a habitat for BHGs to stay for a longerperiod of time. Moreover, probably the most importantresource for the species to survive the winter periodis food. However, this food seems to be patchily dis-tributed within the city. Therefore, use of the terms

‘‘ecological corridor’’ and ‘‘stepping-stones’’ for water-courses and water reservoirs is reasonable when weconsider the foraging behavior of the studied species.

Proximity of the Vistula River in the city center alsohad a positive effect on the presence of birds in the city(Table 1). This part of the river should be considered thesource of individuals from which birds fly to other cityhabitats. The birds often gather at this part of the riverin large numbers (Walasz 2000) and thus they graduallyuse not only this river but also its smaller tributaries andother urban habitats. We think that such large gather-ings of animals near city centers may be a key factor (toour knowledge not considered before), affecting thesynurbanization process of many animals. Such rem-nants of natural habitats, where wildlife and people existin close proximity, may be the starting point at whichbehavioral or even evolutionary processes enable syn-urbanization. However, it must be remembered that typeof food and/or foraging habits are often importantfactors affecting the synurbanization process of birds aswell (Matsubara 2003).

Besides, undoubtedly, the Vistula River itself is alarge ecological corridor used by many other animals atdifferent spatial scales (Gacka-Grzeskiewicz 1995).

The distance to rich food sources (landfill) and localfood resources did not significantly affect the winterpresence of BHGs in the city (Table 1). It is surprising,since the availability of food is often the primary factorin the occurrence of birds during winter (Chamberlainet al. 2007). The availability of waste attracts a numberof species, including BHGs, which congregate in suchplaces in winter (Horton et al. 1983; Belant et al. 1995).It is probable that the city is, on the wider spatial scale,the place where some species gather during winter, buton a local scale within the city, other factors may beresponsible for the presence of the species. It must benoted that the number of BHGs was positively corre-lated with the number of litter-bins (Table 2, Fig. 3b).This indicates that the abundance of this species in ur-ban areas may be affected by the presence of local foodsources (litter-bins), rather than the presence of largelandfills. Jerzak (2001), who examined the abundance ofbreeding Magpies Pica pica in the urban environment,achieved similar results to our own. The number ofMagpies during the breeding season was positively cor-related with the concentration of litter-bins. In our studyarea, BHGs directly benefit from waste food depositedin litter-bins, but they also often forage in their prox-imity by sifting through the garbage previously scatteredby cats or corvids. Moreover, BHGs kleptoparasitizedcorvids or pigeons in order to acquire food. It is possiblethat while moving through the urban environmentBHGs preferentially join foraging flocks of pigeons andcorvids in order to acquire food found by the latterspecies. This, however, requires further research.

None of the factors linked with the negative impact ofhuman disturbance (proximity of communicationarteries, the number of people within the study plots)significantly affected the presence and abundance of

Fig. 3 Factors affecting the abundance of foraging Black-headedGulls in the urban environment in winter. a Mean (with 95%confidence intervals) number of gulls in a given habitat. bRelationship between the number of litter-bins within plots andthe mean number of gulls. c Relationship between distance to thenearest watercourse and mean number of gulls within plots

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BHGs during the winter in the city (Tables 1 and 2).This result may suggest that the process of synurbizationof this species is advanced. However, BHGs are muchmore skittish than urban pigeons or corvids duringforaging (authors’ unpublished data). Nevertheless, wealso recorded several cases where BHGs flew close topeople with food. Moreover, BHGs were seen foragingon windowsills or balconies. Other studies show that thepresence and number of people may have a negativeinfluence on the occurrence, abundance, as well as for-aging behavior of birds (Keller 1991; Burton et al. 2002;Ditchkoff et al. 2006). However, we believe that due toBHG’s opportunistic foraging behavior it may becomeas successful an urban species as corvids are.

Climatic conditions affect utilizationof urban environment by BHGs

Climatic conditions often limit species distribution(Valiela and Bowen 2003; Butler et al. 2007; Adamik and

Pietruszkova 2008; Artemyev 2008). Winter is a criticalperiod for most of the birds as low temperature mayincrease energy demand in a time of usually low foodsupply. Additionally, the presence of snow cover maylimit the access to many food resources. Our study re-vealed that the behavior of the BHGs was significantlyinfluenced by climatic conditions. Higher temperatureand lack of snow cover caused BHGs to use resourcesspread in the urban environment more frequently thanduring more severe climatic conditions. This result isimportant in light of global warming. The urban envi-ronment has an altered energy exchange creating anurban heat island (Gill et al. 2007). The climate change isexpected to amplify this phenomenon (Gill et al. 2007).Therefore, we believe that climate change may speed upthe urbanization process of the BHGs and may intensifypotential conflicts with urban inhabitants. In otherstudies it was shown that birds are sensitive to climatechange and may increase their geographical rangenorthward (Valiela and Bowen 2003). Several bird spe-cies may effectively use energy-rich food in feeding tables

Fig. 4 Climatic conditions anddate affecting the probability ofpresence and abundance offoraging Black-headed Gulls inthe urban environment inwinter. a Mean temperature(with 95% confidence intervals)during surveys when birds werepresent/absent in the plots.b Relationship betweentemperature and numberof gulls within the plots.c Relationship betweenpresence/absence of snow coverand mean number of gullswithin plots. d Relationshipbetween date in the season andnumber of birds within plots

Table 3 Pearson correlation coefficient for continuous variables used in the analyses (N = 240 study plots)

Factor Numberof litter-bins

Distanceto landfill

Distanceto water-course

Distanceto waterreservoirs

Distance tothe VistulaRiver

Averagenumber ofpeople

Distanceto majorarteries

Longitude Latitude

Number of litter-bins 1Distance to landfill 0.053 1Distance to watercourse �0.197** �0.007 1Distance to water reservoirs 0.045 �0.175** 0.130* 1Distance to Vistula River 0.129* 0.009 0.216** 0.130* 1Average number of people �0.094 �0.055 0.105 �0.021 �0.057 1Distance to major arteries 0.096 0.035 0.089 0.027 0.013 0.010 1Longitude 0.042 0.011 0.101 �0.086 �0.074 0.068 0.082 1Latitude 0.107 �0.021 0.001 0.029 0.063 0.069 �0.011 0.091 1

Significant correlations are marked by asterisks: * P < 0.05, ** P < 0.01

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and overcome the problems of severe climate even in thenorth because they winter in cities (Jokimaki et al. 1996;Wilby and Perry 2006). Although our study was notdesigned to test specific hypotheses on climate changeand its long-term effects on population of the BHGs inwinter, the results suggest that climate change may be animportant variable affecting populations of BHGs dur-ing winter in urban environment.

Ways to control large numbers of BHGs in the city

The increasing number of wildlife-human conflicts dueto the growing number of animals colonizing cities hasgiven rise to the need for wildlife management in urbanareas (Rock 2005; Ditchkoff et al. 2006). Gulls in manyurban areas are a public nuisance. Gulls often pollutepublic places, they cause noise, and occasionally displayaggressive behavior towards humans (Calladine et al.2006). Our results suggest that the key factor influencinga utilization of urban environment by studied species isthe presence of corridors and stepping-stones. However,it seems that, at the landscape scale, it would not bereasonable to manage ecological corridors and stepping-stones so as to stop birds moving to urban areas in thewinter. Watercourses and water reservoirs are importantplaces for other, of conservation interest, waterbirds andtherefore should be managed so as to be attractive to thegreatest number of species (Walasz 2000; Manson et al.2006). An effective way to prevent the dispersion ofBHGs in the urban environment would be the creationof habitat patches in the vicinity of ecological corridorsat the city’s borders, which would be a natural source offood for the studied species. These could include variouskinds of green areas such as lawns (Schwemmer et al.2008).

Since the availability of a variety of waste in litter-bins seems to determine the abundance of BHGs, itcould be reasonable that proper construction of thesefacilities, so that it limits access by animals is the bestsolution to the problem of the presence of these birds inresidential areas. For example, litter-bins should haveclosed lids, and refuse heaps should be built in enclosedspaces. This would prevent access to food not only forgulls but also to other undesirable species such as urbanpigeons, corvids, and domestic cats.

Another problem is the feeding of birds by humans inthe winter. Remnants of food are often displayed inplaces visited by BHGs or near refuse heaps, whichmakes the birds favor such places. Some people feedbirds in such a manner in the winter, thus in some placesorganic waste is predictable and an easily accessiblesource of food. The solution to this problem might bethe appropriate education of local communities, espe-cially about the various consequences related to publichygiene and the transmission of disease as the number ofgulls increases in the urban environment. As the largestnumber of gulls in the city is in the middle of winter(Fig. 4d), the action to stop feeding birds as well as

preventing access to litter-bins should be done at thisperiod of time. The impact of feeding BHGs by peopleon the species occurrence in cities should be also ad-dressed in future studies.

Conclusion

Our research shows that BHGs use a variety of habitatsin the city during the winter. However, the use of thecity’s resources by this species depends to a large extenton the presence of aquatic habitats, which are ecologicalcorridors and stepping-stones and local sources of foodsuch as litter-bins. Also, ‘‘sources of individuals’’ wherebirds gather to winter may facilitate the utilization ofurban habitats. Higher temperature and lack of snowcover positively affected utilization of the urban habitatsby the species, which indicates that global warming mayspeed up synurbanization of the BHGs. Further workshould focus primarily on the foraging tactics used bythese birds, and the interactions between gulls and otherspecies wintering in the city. This would help in under-standing what role BHGs play in the urban ecosystem.The effect of climate change on behavior of the species isalso a topic demanding further study.

Acknowledgments The authors gratefully acknowledge KazuhiroEguchi and two anonymous reviewers for their constructive com-ments on the manuscript. This work was supported in part by grantNN304 2370 33 from Polish Ministry of Science and Higher Edu-cation.

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