Science of the Total Environment 823 (2022) 153535 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Gulls living in cities as overlooked seed dispersers within and outside urban environments ⁎ Víctor Martín-Vélez a, , Tomás Montalvo b,c, Isabel Afán a, Antoni Sánchez-Márquez d, Raül Aymí e, Jordi Figuerola a,c, Ádám Lovas-Kiss f, Joan Navarro d a Estación Biológica de Doñana - CSIC, Avenida Américo Vespucio 26, 41092 Sevilla, Spain b Servei de Vigilància i Control de Plagues Urbanes, Agencia de Salud Pública de Barcelona, Pl. Lesseps, 1, 08023 Barcelona, Spain c CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain d Institut de Ciències del Mar – CSIC, Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain e Institut Català d'Ornitologia, Museu de Ciències Naturals de Barcelona, Pl. Leonardo da Vinci, 4-5, 08019, Barcelona, Spain f Wetland Ecology Research Group, Centre for Ecological Research, Institute of Aquatic Ecology, Department of Tisza River Research, Debrecen, Bem tér 18/C. H-4026, Hungary H I G H L I G H T S G R A P H I C A L A B S T R A C T • Urban gulls transport seeds within cities by primary and secondary dispersal. • Seed dispersal through pellet deposition was spatially modelled for the first time. • Seven alien plant species were reported for seed dispersal within Barcelona. • Around 30% of the seeds dispersed were deposited at suitable green urban areas. A R T I C L E I N F O A B S T R A C T Article history: The yellow-legged gull is an opportunistic and generalist bird that has colonised urban areas, where it has found very Received 3 November 2021 favourable trophic resources but also causes disturbance to humans and damage to infrastructure. Here, we investi- Received in revised form 25 January 2022 gated the potential role that gulls play in the dispersal of plants in Barcelona, a highly populated city of north- Accepted 26 January 2022 eastern Spain. We analysed the stomach contents of 145 chicks collected in urban nests and reported the presence Available online 29 January 2022 of seeds of 27 plant taxa. We then developed a plant dispersal model based on the movements of 20 GPS-tracked Editor: Paulo Pereira yellow-legged gulls breeding in the city of Barcelona. We estimated seed dispersal distances, seed shadows and per- centage of seeds reaching habitats suitable for seeds regurgitated in pellets and those excreted in faeces. Seven of Keywords: the 27 plant taxa found in the stomachs were alien taxa to Spain. Average dispersal distances of plant seeds by gulls GPS data were around 700 m, but maximum dispersal distances reached up to 35 km. Dispersal distances and seed spatial pat- Movement ecology terns did not differ between faeces and pellet models, as most strongly depended on gull movements. About 95% of the Green areas seeds were dispersed within urban environments and between 20 and 30% reached suitable habitats for seed deposi- Dispersal distance tion (urban woodlands, green urban parks and urban grasslands). Urban gulls frequently dispersed seeds (including Alien plants alien species) within urban habitats, both via direct consumption or via secondary dispersal after consuming granivo- Urban ecology rous birds that had ingested the seeds, such as pigeons or parakeets. Urban planning for Barcelona is based on native Seed dispersal Yellow-legged gull plant species, and thus, special attention should be paid to alien plants dispersed by birds, which could pose a risk to Larus michahellis native biodiversity in urban ecosystems. ⁎ Corresponding author. E-mail address: victormartin_velez@hotmail.com (V. Martín-Vélez). http://dx.doi.org/10.1016/j.scitotenv.2022.153535 0048-9697/© 2022 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 1. Introduction Seed dispersal within urban landscapes by gulls has never been studied. Barcelona is a good system to study the potential for seed dis- The effects of urbanisation on different bird species are variable (Sol persal and the spatial patterns of seed dispersal deposition within the et al., 2013; Méndez et al., 2020). While many species are unable to city. Furthermore, new technology using GPS tracking devices with adapt to the human impacts associated with cities, others have found a win- yellow-legged gulls in Barcelona can provide reliable bird movements dow of opportunity in city life (McKinney and Lockwood, 1999). Urban information (Méndez et al., 2020) to generate spatial models of seed ecosystems provide stable, accessible food resources and less predation dispersal (e.g. Bartel et al., 2018). In the present study, we aimed to pressure than natural environments for those species able to adapt to cities (1) characterise the plant taxa that can be dispersed by yellow-legged (Lim and Sodhi, 2004; Palomino and Carrascal, 2007; Méndez et al., 2020; gulls breeding and foraging in an urban environment, including Leveau, 2018). Some urban bird species (e.g. house sparrow Passer whether they were alien species and (2) determine the dispersal dis- domesticus) are completely adapted to urban environments without being tances and spatial seed shadows generated by yellow-legged gulls in a nuisance to city managers (Thearle, 2013). However, conflicts with Barcelona. humans are associated with other birds adapted to urban environments, re- sulting from noise pollution, damage to infrastructure and transmission of 2. Materials and methods pathogens (Navarro et al., 2019; Vergara et al., 2017; Senar et al., 2016; Belant, 1997). 2.1. Fieldwork procedures Gulls are a clear example of opportunistic birds adapted to urban envi- ronments both for breeding and foraging (Spelt et al., 2019; Rock et al., The study was developed during the breeding season (May to June) 2016; Méndez et al., 2020). The presence of a wide variety of trophic re- from 2018 to 2021 in the city of Barcelona (north-east Spain, Fig. 1A), a sources, including human-related ones, within cities lead to the establish- coastal urban area considered the eighth and second largest city of ment and growth of urban gull populations worldwide (Washburn et al., Europe and Spain, respectively (1,600,000 inhabitants). The yellow- 2013; Spelt et al., 2019). The number of gulls nesting on roofs is increasing, legged gull urban population of Barcelona has estimated as around 300 creating problems for residents, including defecation, obstruction of drain breeding pairs (Antón et al. 2017). The climate of Barcelona is dry and systems, structural building damage, harassment, airplane collisions and warm in summer and mild and wet during winter with long periods of sun- disease transmission (Belant, 1997; Vidal et al., 1998). Methods for control- light throughout the year. The warmest months- are July and August ling urban gull populations include disturbance to birds, management of (22–28 °C), while January and February (8–11 °C) are the coldest months nesting areas or food sources (from landfills or ports), or direct removal (Algeciras and Matzarakis, 2016). of adult birds (Belant, 1997). To determine the presence of seeds, we analysed the stomach con- Urbanisation is a major factor promoting biological invasions world- tents of 145 chicks of yellow-legged gulls collected in 145 different wide, because highly disturbed habitats provide ecological niches for nests throughout the urban area of Barcelona (Fig. 1B and C). Stomachs alien species. Moreover, cities often act as gateways to alien invasions were frozen at −20 °C until processing in the laboratory. No chicks were through airports, harbours, highways, and train stations, whereas gardens specifically killed for this study because all individuals were provided and urban parks can become sources of propagules for spreading to natural by the Public Health Agency of Barcelona after they were euthanized areas (Farelo et al., 2017). A main feature of the urban flora is the high pro- (Pest Management Plan of Barcelona; Legislative Decree 2/2008 of portion of non-native species (van Heezik et al., 2012). Many alien plant April 15th, DOGC). species were introduced intentionally within the cities for economic and or- To examine the movements of the yellow-legged gulls, during the namental purposes (Czarnecka et al., 2013), and invasive species colonising breeding seasons of 2018 and 2019, 20 breeding adults (that presented in- natural habitats can negatively affect green urban planning efforts cubation patch indicating that were actively breeding) were captured in a (Štajerová et al., 2017; Gaertner et al., 2016). baited trap installed in Barcelona and were tagged with 2 different GPS Zoochorous seed dispersal is another way that non-native species can units (12 individuals tagged with GPS-WIMBISF-25 manufactured by spread. A little-studied impact of gull species in cities is their potential to re- Wimbitek SL and 8 individuals tagged with GPS-CatLog manufactured by distribute plant species both within urban patches and beyond urban envi- Perthold Engineering LLC; Table 1). Each GPS units had different frequency ronments (Calviño-Cancela, 2011). The provisioning of anthropogenic food of GPS data recording (every GPS-WIMBISF-25 30 min for GPS-WIMBISF- resources available in cities such as agricultural crops, orchards, gardens or 25 and 10 or 5 min for GPS-CatLog during 2018 or 2019, respectively). plantations provide exploitable resources to bird species (Sengupta et al., Moreover, the methodology of obtaining the GPS data differed between 2021), with the potential for primary seed dispersal by direct consumption GPS-WIMBISF-25 units (the data was retrieved remotely by using SigFox of seeds or secondary seed dispersal through the consumption of other network) and GPS-CatLog units (the data was downloaded directly from granivorous bird species. Seed dispersal within cities may be especially rel- the logger). All GPS units were deployed using a wing harness (Thaxter evant when the plants dispersed by birds are invasive or alien, as previously et al., 2014). The GPS unit and harness weighed less than 2% of the body stated (Corlett, 2005; Li et al., 2017). mass of the tracked gulls (GPS-WIMBISF-25 = 21 g, GPS-CatLog = 16 g; The yellow-legged gull Larus michahellis is known to disperse a wide va- mean ± SD of instrumented yellow-legged gulls = 1011.23 ± 125.45 g), riety of plants through primary endozoochory (Nogales et al., 2001; below the 3% body mass threshold suggested for gulls (Phillips et al., Calviño-Cancela, 2002). Secondary seed dispersal by the black-backed 2003; Passos et al., 2010). gull Larus fuscus feeding on the American red crayfish Procambarus clarkii (Lovas-Kiss et al., 2018a; Martín-Vélez et al., 2021a) may result in dispersal 2.2. Stomach content analysis distances beyond 150 km for alien and weed plant species (Martín-Vélez et al., 2021b). The proliferation of urban populations of yellow-legged Stomachs were unfrozen and processed under laboratory conditions gulls inhabiting the city of Barcelona can have important implications for during March and December 2021. The stomach contents were inspected seed dispersal, both through direct plant consumption or through second- in Petri dishes and all intact seeds were retrieved, counted, photographed ary seed dispersal (Calviño-Cancela, 2011). In addition to the consumption and measured with ImageJ software (Schneider et al., 2012). We identified of marine resources, urban bird species such as rock pigeon Columba livia them to the lowest taxonomic level by comparing the shape, size and seed and monk parakeet Myiopsitta monachus have been described as important coat pattern to information in the available literature (Bojnanský and prey for this opportunistic gull (Méndez et al., 2020). Rock pigeon and Fargašová, 2007; Cappers et al., 2012). When it was not possible to assign monk parakeet are known to forage on a wide range of urban plant species an item to a species with certainty, genus or family level was reported. (e.g. alien and ornamental species) within cities (Spennemann and Watson, We also classified the identified seeds as native or alien, based on 2017; Borray-Escalante et al., 2020). Aymerich and Sáez (2019). In addition to the seeds, the major prey groups 2 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 Fig. 1. A) Location of Barcelona city within Europe. B) GPS positions (blue circles) of 20 GPS-tracked yellow-legged gulls during the 2018–2019 breeding season in Barcelona. C) Distribution of the 145 nests sampled in Barcelona during the 2019 breeding season to examine the stomach contents of the yellow-legged gull chicks. The draw of yellow legged gull was made by Martí Franch. (e.g. rock pigeon, monk parakeet or fish; Méndez et al., 2020) were identi- 2.3. GPS data analysis fied when possible, photographed and counted (at the smallest number pos- sible). For the spatial movement analysis, we used the following parameters re- corded by the GPS loggers: date, time of day (UTC), latitude, longitude and instantaneous speed, and the body mass of each GPS-tracked gull. We calcu- lated additional variables from the raw parameters: haversine distance be- Table 1 tween fixes, time difference between GPS points (calculated from forward Summary of the data included in the analyses from 20 tagged gull-year individuals intervals between consecutive GPS points set up between 15 and 30 min) breeding in the city of Barcelona during the breeding seasons of 2018 and 2019. In- and trajectory speed (km·h−1). To simulate the start of a gull trajectory, dividual gull identification (ID), GPS model, date of the first and last GPS location, we selected all GPS fixes within the limits of Barcelona city (Fig. 1). Addi- total duration of the track and total number of locations are shown. tionally, we selected only GPS fixes that also overlapped with the distribu- ID GPS Date of first GPS Date of last GPS Total duration Total tion of their main urban prey (rock pigeons and monk parakeets; Anton model location location (days) locations et al., 2017) known to be consumed extensively by yellow-legged gulls PBMM CatTrack 11/05/2018 13/06/2018 33 3126 breeding in Barcelona (Méndez et al., 2020) during the day (from 07:00 PBTP Wimbitek 17/05/2018 30/06/2018 44 1786 to 19:00 h UTC). This time range excluded the main roosting periods and PBWB Wimbitek 17/05/2018 30/06/2018 44 1174 PXTZ Wimbitek 17/05/2018 25/06/2018 39 1405 feeding at sea during night when seed ingestion was less probable. The PXZS CatTrack 09/05/2018 25/06/2018 47 1515 GPS fixes within Barcelona under those requirements correspond to a PYAB CatTrack 26/04/2018 09/05/2018 13 1219 total of 706 gull-day trajectories from a combination of the 20 tracked PYFL CatTrack 11/06/2018 30/06/2018 19 1885 gulls (Table 1). PYHS CatTrack 26/04/2018 30/04/2018 4 402 PZYL CatTrack 04/06/2018 30/06/2018 26 2533 PBLZ Wimbitek 08/05/2019 30/05/2019 22 842 2.4. Seed deposition modelling PBMM Wimbitek 01/04/2019 30/06/2019 90 1540 PBSF CatTrack 10/04/2019 15/05/2019 35 4337 Faeces deposition was simulated based on a seed retention curve de- PBWB Wimbitek 08/04/2019 30/06/2019 83 1886 rived from an allometric equation (Eq. (1)) which relates mean retention PXJS Wimbitek 07/05/2019 30/06/2019 54 2035 PXMC Wimbitek 26/04/2019 30/06/2019 65 2849 time to body mass across bird species (Yoshikawa et al., 2019): PXXT Wimbitek 05/04/2019 23/06/2019 79 2494 PXZY Wimbitek 26/04/2019 30/04/2019 4 207 PZZC CatTrack 30/04/2019 18/05/2019 18 5073 Log10 mean seed retention time ð minÞ PXXT Wimbitek 09/04/2019 15/05/2019 36 620 ¼ 0:631 þ 0:561  log10 body mass ðgÞ: ð1Þ 3 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 We used a mean and standard deviation body mass of 1006 ± 136 g model for a correct visualization. We used the Point Density tool from (based on the body mass of the 20 GPS-tracked yellow-legged gulls), and ArcMap 10.1 with a final spatial resolution of 10 m. We calculated seed den- extracted a mean retention time of 3.44 h (Eq. (1)). We then generated a sity maps for each model separately (pellet and faeces) and then summed the lognormal retention time distribution from a shape (sdlog) and a scaling two outputs to perform a final model based on pellets and excrement to- (meanlog) parameter (Viana et al., 2016). The scaling parameter was calcu- gether. Areas with a high probability of seed deposition were selected by con- lated from the mean retention time derived from Eq. (1), and the shape pa- sidering those areas enclosing the 25%, 50% and 75% quantile values from rameter is fixed at 0.7 (using the rlnorm function in R by random the final seed model. Furthermore, crossed this seed deposition map generation), as proposed by Viana et al. (2016) for endozoochory relation- with the land use information (scale 1:2000, year 2020) from Catalonia ships (Fig. 2). (Ibáñez et al., 2002). This allowed us to determine the seven main hab- One of the 706 gull-days was randomly selected and assumed that the itat types into which seeds would be dispersed: (1) port, (2) waste seed ingested at time t0 was randomly assigned to an hour between 07:00 dump, (3) beach and sea, (4) urban woodland, (5) green urban area, and 19:00 h. Based on the retention time curve, we randomly selected a re- (6) other urban area and (7) grassland. From these, we only considered tention time t1 when the seed would be excreted, based on the density prob- urban woodland, green urban area and grassland as potential areas suit- ability curve through the sample function in R (v3.6.3 R Core Team, 2020). able for successful seed establishment after dispersal. Finally, areas with The location of seed egestion was calculated based on the GPS coordinates higher probability of successful dispersal were delimited as those previ- at t1, and the Haversine distance between GPS points at t0 and t1 where the ous areas with a high probability of seed deposition that had habitats seed was dispersed was calculated through deg.dist function in fossil R pack- suitable for seed establishment. The software ArcMap 10.1 (ESRI, age. We performed the modelling to simulate pellet deposition from t0 until Redland, USA) and RStudio 4.0.3 (RStudio Team, 2020) were used to t1, with pellet deposition t1 being the first GPS point from the random tra- perform this spatial analysis. jectory when the gull was resting and not flying and beyond 9.5 h, the time that yellow-legged gulls take to produce animal pellets in captivity (Nogales 3. Results et al., 2001). We repeated these randomizations 1000 times for each excre- ment and pellet modelling and assumed each excreta contained 1 intact 3.1. Stomach contents seed. Therefore, each model simulation represented the dispersal of 1000 seeds in the study area. Differences between dispersal distances in seed Of the 145 stomachs analysed, 91 (63%) contained rock pigeon, 63 models were analysed through Wilcoxon U non-parametric test being α (43%) contained fish and 19 (13%) contained signs of small rodents. = 0.05. Each faeces accounts only for 12.5% of total daily faecal output There were signs of garbage (mainly plastic) but no invertebrates. Forty- in gulls (Hahn et al., 2007), and the number of gulls in Barcelona is above five out of the 145 stomachs analysed (31%) contained seeds, 30 of 1000 (Anton et al., 2017). Therefore, faecal simulation represented only a which (66.7%) also contained rock pigeons. An average of 0.85 seeds per fraction (roughly 25%) of the number of viable seed dispersal events by stomach was found with a maximum of four different plant taxa found in yellow-legged gulls in a day. two samples. A total of 27 different plant taxa and 124 seed items were We generated a spatially explicit seed deposition map in the city. First, we found in the stomach samples, seven of them considered species alien to generated a density map (in seeds km−2) considering a 100 m neighbouring Spain (Table 2). Twenty-one of the ten taxa were associated with rock pi- area of influence around each seed deposition point estimated from the geon remains in the stomach samples (Table 2). Rarefaction analyses re- vealed a steep slope, suggesting that increasing sample size will increase the number of plant species present in the stomach content of yellow- legged gull chicks (Fig. S1). 3.2. Seed dispersal modelling We did not find differences in the dispersal distances recorded between the 20 GPS-tracked yellow-legged gulls (Wilcox chi-squared = 511,272, p = 0.32). The mean dispersal distance of 1000 seeds from randomizations based on faecal retention times was 0.77 km with a maximum of 35.71 km (Table 3, Fig. 3). Mean dispersal distance for seeds egested via pellets was 0.86 km with a maximum of 35.68 km (Table 3, Fig. 3). Median distance was 0.07 km for faeces model and 0.07 km for pellets model (Table 3; Fig. 3). Approximately 95% of the seeds deposited by both faeces and pellet models fell within Barcelona city boundaries. Areas with the highest densi- ties of deposited seeds (up to 12,095 seeds km−2) were restricted to an urban park area within Barcelona city, where adults were captured (Fig. 4A) and the areas close to an urban hill and a fishing and industrial port area (Fig. 4B). Sixty percent of the highest density area (25% quantile corresponding to the red area in Fig. 4) was related to other urbanised hab- itats, whereas approximately 20 and 10% were related to woodland urban areas and green urban areas, respectively (Table 4). Fifty-two percent of the total modelled seeds dispersed by either pellets or faeces were de- posited within the urban area of Barcelona not suitable for seed estab- lishment. However, around 20% of the seed densities fell within a suitable green area within Barcelona, including urban woodland Fig. 2. Theoretical curve based on 3.44 h mean retention time (calculated from (9.8%), grasslands (3.37%) and green urban zone (7.01%) (Table 4). Eq. (1)) and a lognormal curve with sdlog = 0.7 corresponding to the shape of The remaining seeds were deposited within the Barcelona port at the the curve derived from random sampling (N = 100) (after Viana et al., 2016). beach or directly at sea (2.1% of the total seeds). Seeds that travelled Red dashed lines indicate the mean retention time estimated from the random the farthest (1.91% of them) were deposited in a dump, 35 km away generation as 4.1 h (with shape 0.7). from Barcelona city (Fig. 4C). 4 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 Table 2 Details of the taxa of plants with intact seeds found in the stomachs of the chicks of yellow-legged gulls sampled from 2018 to 2021 in the city of Barcelona. For each taxon, the association with a prey item (e.g. rock pigeon), the native status of the plant taxa to Spain according to Aymerich and Sáez (2019), the number of samples in which the taxon was recorded (NST), the combined number of seeds in those samples (N total seeds) and the maximum of seeds recorded per taxa is given. Family Species Presence of Native NST N of Max seed bird as prey species seeds per sample Actinidiaceae Actinidia deliciosa No No 1 1 1 Arecaceae Washingtonia robussta Yes No 2 10 9 Brassicaceae Coronopus squamatus Yes Yes 1 14 14 Brassicaceae – Yes – 1 1 1 Cannabaceae Celtis australis No Yes 1 1 1 Convolvulaceae Cuscuta cf. campestris Yes No 2 6 3 Cucurbitaceae – Yes – 1 1 1 Tetragonolobus Fabaceae maritimus Yes Yes 2 6 4 Fabaceae Trifolium repens Yes Yes 1 1 1 Fabaceae Trifolium sp. Yes – 1 2 2 Juncaceae Juncus sp. No – 1 3 3 Lythraceae Lythrum cf. salicaria No Yes 1 1 1 Moraceae Ficus carica Yes No 1 1 1 Oleaceae Olea europaea Yes Yes 3 3 1 Plantaginaceae Veronica sp. Yes – 2 1 1 Poaceae Setaria viridis Yes Yes 1 1 1 Poaceae Echinochloa cruss-galli Yes No 8 52 37 Poaceae Echinochloa sp. Yes – 1 1 1 Poaceae Oryza sativa Yes Yes 1 1 1 Polygonaceae Polygonum aviculare No Yes 1 1 1 Ranunculaceae Ranunculus arvensis Yes Yes 1 3 3 Fig. 3. Cumulative frequency distributions of dispersal distances (km) obtained Ranunculus from excreta models build using faeces (solid line) and pellet (dashed line) Ranunculaceae trichophyllus No Yes 1 3 3 retention time curves, with a log scale on the X-axis based on 1000 random seeds Ranunculaceae Ranunculus baudotii Yes Yes 1 1 1 modelled. Rubiaceae Galium sp. Yes – 2 3 2 Solanum Solanaceae chenopodioides Yes No 1 1 1 Given the small size of the seeds dispersed and the abundant prey item re- Solanaceae Solanum eleagnifolium Yes No 1 1 1 mains in the samples, a secondary seed dispersal mechanism is the most Urticaceae Urtica dioca Yes Yes 1 4 4 Total 124 likely explanation, as has been reported previously for other gull species (e.g. Larus fuscus; Lovas-Kiss et al., 2018a). On the other hand, Ficus carica, Actinidia deliciosa, Oliva europaea, Celtis australis, Washingtonia robussta and 4. Discussion Solanum spp. present fleshy fruits which may be ingested actively by yellow-legged gulls. Other studies have reported an active ingestion of In the present study, we present for the first time a spatial analysis of the other fleshy fruits by gulls (e.g. Ruppia fruticosa, Corema album; Nogales seed shadows and dispersal services provided by an urban living population et al., 2001, Calviño-Cancela, 2002), olives (Calviño-Cancela, 2011), and of yellow-legged gulls. While this dispersal service may have positive ef- they have been observed consuming fruits of Washingtonia robusta in Barce- fects on the maintenance of connectivity and biodiversity, it also has poten- lona (Raül Aymí, personal observation, Fig. S2). tial negative effects because many of the dispersed plant species were alien, Unfortunately, we could not test the viability of these seeds in the cur- some with invasive potential presenting a possible risk for natural habitats. rent study because the gull stomachs were frozen for months before analy- sis. Previous studies have reported that many of the plant species reported 4.1. Stomach contents and seed dispersal potential in this study were previously dispersed by other birds. For example, Ficus carica was reported in faecal samples of mallards (Anas platyrhynchos) and The rock pigeon was the most frequently identified prey item followed ravens (Corvus corax) (Lovas-Kiss et al., 2018b; Nogales et al., 1999). by fish remains, as previously reported by Méndez et al. (2020) for the same Echinochloa cruss-galli was reported germinate after being dispersed by mal- area in previous years. The main novelty of our study is the detection of sec- lards (Wongsriphuek et al., 2008). Trifolium repens was reported to be sec- ondary dispersion of seeds by yellow-legged gulls. Moreover, 78% plant ondarily dispersed by white storks through pellets (Martín-Vélez et al., taxa reported in the study were found together with urban bird remains 2021a). Plant species from the genera Solanum spp. and Ranunculus spp. that served as prey for gulls. Most of the plant species reported do not germinated after being secondarily dispersed by lesser black-backed gulls have a fleshy fruit, supporting previous evidence that gulls are effective Larus fuscus in South Spain (Lovas-Kiss et al., 2018a; Martín-Vélez et al., seed dispersers of non-fleshy fruited plants (Martín-Vélez et al., 2021a). 2021a). Therefore, the potential for those plant species to be successfully dispersed by yellow-legged gulls in Barcelona is very high. Table 3 4.2. Model comparison and dispersal distances Comparison between models builds from faeces and pellet retention time curves, presenting dispersal distances (in km, means, quantiles and maximum distances). Models parametrised for faecal and pellet dispersal generated similar Note 50% quantiles are the medians. dispersal distances for yellow-legged gulls. To the best of our knowledge Model Dispersal distance (km) these are the first spatial dispersal seed shadows generated for pellets, as previous seed dispersal models based on GPS movements in waterbirds Mean 25% 50% 75% Max were focussed only on faeces deposition (Martín-Vélez et al., 2021b; Faeces 0.77 0.02 0.07 0.39 35.71 Kleyheeg et al., 2017). Here, we show that pellet dispersal distances may Pellet 0.86 0.02 0.07 0.40 35.68 be as far as faecal deposition distances, with pellets being an important 5 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 Fig. 4. Density of seeds dispersed based on a combined faecal and pellet deposition simulation models (1000 seeds each) and on the GPS trajectories of 20 yellow-legged gulls. Coloured areas show the estimated point density of seeds deposited, with red areas representing the highest seed densities and the 25% quantile, orange areas the 50% quantile and yellow areas the 75% quantile. Uncoloured areas reflect zero seed density. (A) Zoom-in of the highest density area within Barcelona city corresponding to Ciutadella Park. (B) Zoom-in of the Montjuïc urban hill park and Barcelona port. (c) Seeds deposited beyond Barcelona limits in a dump. mechanism for seed dispersal (Padilla et al., 2012). In fact, gull chicks are 100 m) reported here were lower than distances reported in previous spa- fed by breeding gulls via pellets (Moreno et al., 2010), so the plant taxa tial seed dispersal models parameterised with movement data of birds in list reported and the seed dispersal patterns generated from the pellet natural environments. Kleyheeg et al. (2017) reported median dispersal dis- model may be more reliable. tances for mallards Anas platyrhynchos between 600 and 3000 m, whereas The seed dispersal distance quantified by our models showed average Martín-Vélez et al. (2021b) reported dispersal distances for the lesser dispersal distances of 770 m. The median dispersal distances (close to black-backed gull between 700 and 900 m with maximum dispersal dis- tances greater than 150 km. The shorter seed dispersion distances found in our study may be due to the adaption of gulls to urban environments, where human refuse may provide predictable resources for chick rearing Table 4 (Spelt et al., 2019) near the breeding places inside the city. Furthermore, Habitat composition (in percentages) of the areas with higher densities of seeds dis- gull mobility and distance travelled during breeding are lower than in the persed by yellow-legged gulls in Barcelona city. Percentage of habitat types was cal- non-breeding period (Shamoun-Baranes et al., 2017; Ramírez et al., culated for 25% (Q25), 50% (Q50) and 75% (Q75) quantiles of seed deposition density maps, based on both faecal and pellet deposition. Note that quantiles are as- 2020). Future studies including non-breeding season will be necessary to sociated with colours from Fig. 4. understand the entire gull movements and thus, the complete seed dispersal shadows. Nevertheless, the importance of seed dispersion by gulls should Density area Q25% Q50% Q75% All seeds not be underestimated. Several hundreds of seeds may be dispersed over Suitable areas for seed establishment 33.14% 26.25% 23% 20.18% distances exceeding 1 km on a daily basis by the yellow-legged gull popula- Urban woodland 19.95 16.05 12.45 9.8 Grassland 3.3 0.9 1.6 3.37 tion within and beyond Barcelona boundaries. Unlike random dispersal by Green urban area 9.88 9.3 8.95 7.01 wind or water, bird dispersal is more likely to transport many terrestrial seeds to locations that are favourable for germination. Unsuitable areas for seed establishment 66.86% 73.75% 77% 79.82% Other urban area 60.24 57.59 55.38 51.8 Dispersal models estimated dispersal distances since other urban bird Port 6.62 15.54 18.73 23.34 prey were consumed, but we have no information regarding the distance al- Sea/beach – 0.04 2.1 2.77 ready travelled for primary dispersers. Total distance dispersal kernels Waste dump – 0.61 0.82 1.91 should also take into account the movements of the primary consumers Total 100 100 100 100 (Rogers et al., 2019). In this sense, dispersal distances modelled for gulls 6 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 may not reflect the entire dispersal distance of the plant species. Despite 5. Conclusions this, the gull's main prey, the pigeon, is a sedentary bird with little mo- bility and a home range of about 550 m, so that the total dispersal dis- Urban yellow-legged gulls may play an unrecognized role in the seed tance would not be greatly increased. On the other hand, maximum dispersal of both plants with fleshy fruit through primary dispersal and dispersal distances were associated with a nearby dump located about plants lacking fleshy fruit via secondary dispersal by granivorous bird con- 35 km from Barcelona. Waste dumps are typical foraging habitats for sumption. The seed shadows predicted from seed retention curves and gull gulls, so the possibility that gulls ingested seeds before flying to the movements indicate that gulls can disperse around 20–30% of seeds be- dump is uncertain, and this may have overestimated the seed dispersal tween green urban areas. Seven of the plants dispersed are considered densities around the waste dump. alien species, and gulls may increase the risk of dispersal of these alien spe- cies. Urban planning for Barcelona is based on native plant species, and spe- 4.3. Seed dispersal across habitats and urban green planning cial attention should be paid to alien plants dispersed by birds, which could pose a risk to natural habitats in urban ecosystems. Urban areas are a mosaic of vegetation patches with varying degrees of connectivity embedded within a built environment matrix (Gelmi- CRediT authorship contribution statement Candusso and Hämäläinen, 2019). The majority of the seeds were de- posited within the Barcelona city boundaries. Seeds outside Barcelona VMV wrote the first draft of the manuscript and performed data analy- boundaries were deposited either at the waste dump or at the sea ses; TM collected the field data and reviewed the manuscript; IF contributed close to the port facilities. Seed deposition within Barcelona boundaries to designing the methodology, contributed to data interpretation and re- was expected given the dominance of gull trajectories within the city, viewed the manuscript several times; ASM collected the laboratory data; which remained close to their nests and the Ciutadella park, near the RA collected the field data; JF contributed to problem conceptualization, area of capture. Due to the high mobility across the city, it is also ex- methodology and to improving the manuscript; ALK identified the plant pected that many seeds were deposited within urban areas that were taxa and reviewed the manuscript; JN conceived the idea, contributed to not suitable for plant establishment. However, between 20 and 30% of methodology design and reviewed the manuscript several times. the seeds are estimated to be deposited within green areas in Barcelona, including urban woodland, grasslands and green urban areas (e.g. Availability of data parks), concentrated within the Ciutadella park and the surroundings of Montjuïc (Fig. 4A–B). Monjuïc is a mountain situated on the south- Data will be uploaded to CSIC repository. west of the city (3.6 km2). It is a main touristic hotspot with over 17 mil- lion visitors annually. Moreover, it is partly surrounded by a railway, ex- Declaration of competing interest pressway, and is next to the seaport. Many initiatives in different cities aim to increase and manage urban The authors declare that they have no known competing financial inter- parks, gardens and nature reserves to facilitate biodiversity conservation ests or personal relationships that could have appeared to influence the and promote landscape connectivity (Horta et al., 2018; Pla Natura, work reported in this paper. 2021-2030). At a time of unprecedented environmental change, including ongoing biodiversity loss, urban landscapes need to reflect local environ- Acknowledgements mental conditions to preserve the future of the natural environment. Barce- lona is a reference city which has developed a green plan to enhance urban Thanks to the staff of the Zoo of Barcelona, especially Pablo Cermeño and biodiversity by promoting and protecting native plant species and enhanc- Camilo Iriondo, for their help in the trapping procedures. Marc Vez helped ing green connectivity by creating a green areas network (Ajuntament de during the stomach content analyses. This study is part of the BCN-Gulls pro- Barcelona, 2013; Parés et al., 2016). National and European directives ject funded by the Barcelona Zoo Foundation and the Ramón y Cajal project and The Territorial Metropolitan Plan of Barcelona (TMPB) aim to include (RYC-2015-17809) and the JAEIntro-ICU (CSIC) of A.S.-M. This work biodiversity conservation and the improvement of ecosystem services in acknowledges the ‘Severo Ochoa Centre of Excellence’ accreditation urban planning and in the design of green infrastructure (Basnou et al., (CEX2019-000928-S). János Bolyai Research Scholarship of the Hungarian 2020). Future Barcelona nature plan directives for 2021–2030 involve the Academy of Sciences, and the New National Excellence Programme of the conservation of natural heritage by preventing species and habitat lost, en- Ministry of Innovation and Technology ÚNKP-21-5, NKFIH OTKA FK- hancing green connectivity and creating a more resilient city to face climate 127939 and FK 138698 grants (ÁLK). All fieldwork was approved by the change, among other efforts (Pla Natura, 2021-2030). Ethics Committee of ICM-CSIC, in accordance with the Spanish and EU leg- In this study, seven plant taxa (Ficus carica, Echinochloa cruss-galli, Sola- islation on the protection of animals used for scientific purposes. num chenopodioides, Solanum eleagnifolium, Actinia deliciosa, Washingtonia robussta, Cuscuta cf. campestris) were non-native to Spain (Aymerich and Appendix A. Supplementary data Sáez, 2019). Echinochloa cruss-galli is an important weed species in agricul- tural landscapes, with adaptive characteristics to survive and over compete Supplementary data to this article can be found online at https://doi. other plant species (Bajwa et al., 2015). Solanum eleagnifolium is considered org/10.1016/j.scitotenv.2022.153535. one of the worse alien plant species within Europe due to its capacity for spreading and establishment, and previously assumed to be dispersed by References abiotic means (Vladimirov et al., 2015). Therefore, seed dispersal between green urban areas by gulls may become a “disservice” if those alien plant Ajuntament de Barcelona, 2013. Barcelona green infrastructure and biodiversity plan 2020 species are transported (Wenny et al., 2016), interfering with urban plans [online report]. www.ajuntament.barcelona.cat/ecologiaurbana/sites/default/files/B to promote native flora within urban environments. If alien species domi- arcelona%20green%20infrastructure%20and%20biodiversity%20plan%202020.pdf nate in urban areas, the gulls have the potential to disperse their seeds to Accessed 20 January 2016. Algeciras, J.A.R., Matzarakis, A., 2016. Quantification of thermal bioclimate for the manage- natural and rural areas in the neighbourhood of the cities. City managers ment of urban design in Mediterranean climate of Barcelona, Spain. Int. J. Biometeorol. should consider that non-native plants used in urban green patches may 60 (8), 1261–1270. be dispersed by birds, another reason to favour native vegetation over Anton, M., Herrando, S., Garcia, D., Ferrer, X., Cebrian, R., 2017. Atles dels ocells nidificants non-native species in urban planning. Special attention should be paid to de Barcelona. Ajuntament de Barcelona/ICO/UB/Zoo. Barcelona. Aymerich, P., Sáez, L., 2019. Checklist of the vascular alien flora of Catalonia (northeastern Ciutadella Park and its surroundings, as a higher density of seeds is ex- Iberian Peninsula, Spain). Mediterr. Bot. 40 (2), 215–242. https://doi.org/10.5209/ pected to be deposited via yellow-legged gulls in this area. mbot.63608. 7 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 Bajwa, A.A., Jabran, K., Shahid, M., Ali, H.H., Chauhan, B.S., 2015. Eco-biology and manage- Navarro, J., Grémillet, D., Afán, I., Miranda, F., Bouten, W., Forero, M.G., Figuerola, J., 2019. ment of echinochloa crus-galli. Crop Prot. 75, 151–162. https://doi.org/10.1016/j. Pathogen transmission risk by opportunistic gulls moving across human landscapes. Sci. cropro.2015.06.001. Rep. 9 (1), 1–5. https://doi.org/10.1038/s41598-019-46326-1. Bartel, R.D., Sheppard, J.L., Lovas-Kiss, A., Green, A.J., 2018. Endozoochory by mallard in Nogales, M., Hernández, E.C., Valdés, F., 1999. Seed dispersal by common ravens Corvus New Zealand: what seeds are dispersed and how far? PeerJ 6, e4811. https://doi.org/ corax among island habitats (Canarian Archipelago). Ecoscience 6 (1), 56–61. https:// 10.7717/peerj.4811. doi.org/10.1080/11956860.1999.11952193. Basnou, C., Baró, F., Langemeyer, J., Castell, C., Dalmases, C., Pino, J., 2020. Advancing the Nogales, M., Medina, F.M., Quilis, V., González-Rodríguez, M., 2001. Ecological and biogeo- green infrastructure approach in the province of Barcelona: integrating biodiversity, eco- graphical implications of yellow-legged gulls (Larus cachinnans Pallas) as seed dispersers system functions and services into landscape planning. Urban For. Urban Green. 55, of Rubia fruticosa ait. (Rubiaceae) in the Canary Islands. J. Biogeogr. 28 (9), 1137–1145. 126797. https://doi.org/10.1016/j.ufug.2020.126797. https://doi.org/10.1046/j.1365-2699.2001.00622.x. Belant, J.L., 1997. Gulls in urban environments: landscape-level management to reduce conflict. Padilla, D.P., González-Castro, A., Nogales, M., 2012. Significance and extent of second- Landsc. Urban Plan. 38, 245–258. https://doi.org/10.1016/S0169-2046(97)00037-6. ary seed dispersal by predatory birds on oceanic islands: the case of the canary archi- Bojnanský, V., Fargašová, A., 2007. Atlas of Seeds and Fruits of Central and East-European pelago. J. Ecol. 100 (2), 416–427. https://doi.org/10.1111/j.1365-2745.2011. Flora: The Carpathian Mountains Region. Springer, Berlin. 01924.x. Borray-Escalante, N.A., Mazzoni, D., Ortega-Segalerva, A., Arroyo, L., Morera-Pujol, V., Palomino, D., Carrascal, L.M., 2007. Habitat associations of a raptor community in a mosaic González-Solís, J., Senar, J.C., 2020. Diet assessments as a tool to control invasive species: landscape of Central Spain under urban development. Landsc. Urban Plan. 83, comparison between Monk and Rose-ringed parakeets with stable isotopes. J. Urban Ecol. 268–274. https://doi.org/10.1016/j. landurbplan.2007.04.011. 6 (1), juaa005. https://doi.org/10.1093/jue/juaa005. Parés, M., de Biodiversitat, C.D.P., Rull, C., de Biodiversitat, T.D.P., 2016. Spain: Developing Calviño-Cancela, M., 2002. Spatial patterns of seed dispersal and seedling recruitment in the Barcelona Green Infrastructure and Biodiversity Plan. Nature-based Solutions to Ad- Corema album (Empetraceae): the importance of unspecialized dispersers for regenera- dress Global Societal Challenges, p. 72. tion. J. Ecol., 775–784 https://doi.org/10.1046/j.1365-2745.2002.00711.x. Passos, C., Navarro, J., Giudici, A., González-Solís, J., 2010. Effects of extra mass on the pe- Calviño-Cancela, M., 2011. Gulls (Laridae) as frugivores and seed dispersers. Plant Ecol. 212 lagic behavior of a seabird. Auk 127 (1), 100–107. https://doi.org/10.1525/auk.2009. (7), 1149–1157. https://doi.org/10.1007/s11258-011-9894-2. 09036. Cappers, R.T., Bekker, R.M., Jans, J.E., 2012. Digitale Zadenatlas van Nederland/Digital seed Phillips, R.A., Xavier, J.C., Croxall, J.P., 2003. Effects of satellite transmitters on albatrosses atlas of the Netherlands. Vol. 4. Barkhuis, Groningen. and petrels. Auk 120 (4), 1082–1090. https://doi.org/10.1093/auk/120.4.1082. Corlett, R.T., 2005. Interactions between birds, fruit bats and exotic plants in urban Hong Pla Natura, 2021-2030. Barcelona. https://www.decidim.barcelona/processes/PlaNaturaBCN? Kong, South China. Urban Ecosyst. 8 (3), 275–283. https://doi.org/10.1007/s11252- participatory_process_slug=PlaNaturaBCN Accessed 29/09/2021. 005-3260-x. R Core Team, 2020. R: A language and environment for statistical computing. R Foundation Czarnecka, J., Kitowski, I., Sugier, P., Mirski, P., Krupiński, D., Pitucha, G., 2013. Seed dis- for Statistical Computing, Vienna, Austria. https://www.R-project.org/. persal in urban green space–does the rook Corvus frugilegus L. contribute to urban Ramírez, F., Afán, I., Bouten, W., Carrasco, J.L., Forero, M.G., Navarro, J., 2020. Humans flora homogenization? Urban For. Urban Green. 12 (3), 359–366. https://doi.org/10. shape the year-round distribution and habitat use of an opportunistic scavenger. Ecol. 1016/j.ufug.2013.03.007. Evol. 10, 4716–4725. https://doi.org/10.1002/ece3.6226. Farelo, P., Gómez-Bellver, C., Montserrat, J.M., Pyke, S., López-Pujol, J., Ibáñez Cortina, N., Rock, P., Camphuysen, C.J., Shamoun-Baranes, J., Ross-Smith, V.H., Vaughan, I.P., 2016. Re- 2017. Montjuïc Mountain (Barcelona, Spain): A" natural" laboratory for plant invasions? sults from the first GPS tracking of roof-nesting herring gulls Larus argentatus in the UK. XIX International Botanical Congress (2017) . http://hdl.handle.net/10261/196779 Ringing Migr. 31 (1), 47–62 10.1080/ 03078698.2016.1197698. Gaertner, M., Larson, B.M., Irlich, U.M., Holmes, P.M., Stafford, L., van Wilgen, B.W., Rogers, H.S., Beckman, N.G., Hartig, F., Johnson, J.S., Pufal, G., Shea, K., Zambrano, J., 2019. Richardson, D.M., 2016. Managing invasive species in cities: a framework from Cape The total dispersal kernel: a review and future directions. AoB Plants 11 (5), plz042. Town, South Africa. Landsc. Urban Plan. 151, 1–9. https://doi.org/10.1016/j. https://doi.org/10.1093/aobpla/plz042. landurbplan.2016.03.010. RStudio Team, 2020. RStudio: integrated development for R. URLRStudio, PBC, Boston, MA. Gelmi-Candusso, T.A., Hämäläinen, A.M., 2019. Seeds and the city: the interdependence of http://www.rstudio.com/. zoochory and ecosystem dynamics in urban environments. Front. Ecol. Evol. 7, 41. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH image to ImageJ: 25 years of image https://doi.org/10.3389/fevo.2019.00041. analysis. Nat. Methods 9, 671–675. Hahn, S., Bauer, S., Klaassen, M., 2007. Estimating the contribution of carnivorous waterbirds Senar, J.C., Domènech, J., Arroyo, L., Torre, I., Gordo, O., 2016. An evaluation of monk par- to nutrient loading in freshwater habitats. Freshw. Biol. 52 (12), 2421–2433. https://doi. akeet damage to crops in the metropolitan area of Barcelona. Anim. Biodivers. Conserv. org/10.1111/j.1365-2427.2007.01838.x. 39 (1), 141–145. https://doi.org/10.32800/abc.2016.39.0141. Horta, M.B., Bhakti, T., Cordeiro, P.F., Carvalho-Ribeiro, S.M., Fernandes, G.W., Goulart, F.F., Sengupta, A., McConkey, K.R., Kwit, C., 2021. The influence of provisioning on animal- 2018. Functional connectivity in urban landscapes promoted by Ramphastos Toco (Toco mediated seed dispersal. Oikos https://doi.org/10.1111/oik.08276. Toucan) and its implications for policy making. Urban Ecosyst. 21 (6), 1097–1111. Shamoun-Baranes, J., Burant, J.B., van Loon, E.E., Bouten, W., Camphuysen, C.J., 2017. https://doi.org/10.1007/s11252-018-0789-z. Short distance migrants travel as far as long distance migrants in lesser black- Ibáñez, J.J., Burriel, J.A., i Pons, X., 2002. El mapa de cobertes del sòl de Catalunya: una eina backed gulls Larus fuscus. J. Avian Biol. 48 (1), 49–57. https://doi.org/10.1111/ per al coneixement, la planificació i la gestió del territori. Perspectivas Territorials. 3. jav.01229. Departament de Política Territorial i Obres Públiques, Generalitat de Catalunya, Barce- Sol, D., Lapiedra, O., González-Lagos, C., 2013. Behavioural adjustments for a life in the lona, pp. 10–25. city. Anim. Behav. 85 (5), 1101–1112. https://doi.org/10.1016/j.anbehav.2013.01. Kleyheeg, E., Treep, J., de Jager, M., Nolet, B.A., Soons, M.B., 2017. Seed dispersal distribu- 023. tions resulting from landscape-dependent daily movement behaviour of a key vector spe- Spelt, A., Williamson, C., Shamoun-Baranes, J., Shepard, E., Rock, P., Windsor, S., 2019. Hab- cies, Anas platyrhynchos. J. Ecol. 105 (5), 1279–1289 10.1111/ 1365-2745.12738. itat use of urban-nesting lesser black-backed gulls during the breeding season. Sci. Rep. 9, Leveau, L.M., 2018. Urbanization, environmental stabilization and temporal persistence of 10527 10. 1038/s41598-019-46890-6. bird species: a view from Latin America. PeerJ 6, e6056. https://doi.org/10.7717/ Spennemann, D.H.R., Watson, M.J., 2017. Dietary habits of urban pigeons (Columba livia) peerj.6056. and implications of excreta pH – a review. Eur. J. Ecol. 3 (1), 27–41. https://doi.org/ Li, N., Yang, W., Fang, S., Li, X., Liu, Z., Leng, X., An, S., 2017. Dispersal of invasive Phytolacca 10.1515/eje-2017-0004. Americana seeds by birds in an urban garden in China. Integr. Zool. 12 (1), 26–31. Štajerová, K., Šmilauer, P., Brůna, J., Pyšek, P., 2017. Distribution of invasive plants in urban https://doi.org/10.1111/1749-4877.12214. environment is strongly spatially structured. Landsc. Ecol. 32 (3), 681–692. https://doi. Lim, H.C., Sodhi, N.S., 2004. Responses of avian guilds to urbanisation in a tropical city. org/10.1007/s10980-016-0480-9. Landsc. Urban Plan. 66, 199–215 10. 1016/S0169-2046(03)00111-7. Thaxter, C.B., Ross-Smith, V.H., Clark, J.A., Clark, N.A., Conway, G.J., Marsh, M., ... Lovas-Kiss, Á., Sánchez, M.I., Molnár, V.A., Valls, L., Armengol, X., Mesquita-Joanes, F., Burton, N.H., 2014. A trial of three harness attachment methods and their suitability Green, A.J., 2018a. Crayfish invasion facilitates dispersal of plants and invertebrates by for long-term use on Lesser Black-backed Gulls and Great Skuas. Ringing Migr. 29 (2), gulls. Freshw. Biol. 63 (4), 392–404. https://doi.org/10.1111/fwb.13080. 65–76. Lovas-Kiss, Á., Vizi, B., Vincze, O., Molnár, V.A., Green, A.J., 2018b. Endozoochory of aquatic Thearle, R.J.P., 2013. Urban bird problems. The Problems of Birds as Pests: Proceed- ferns and angiosperms by mallards in Central Europe. J. Ecol. 106 (4), 1714–1723. ings of a Symposium Held at the Royal Geographical Society, London, on. Vol. https://doi.org/10.1111/1365-2745.12913. 28, p. 181. Martín-Vélez, V., Lovas-Kiss, Á., Sánchez, M.I., Green, A.J., 2021a. Endozoochory of the same van Heezik, Y., Dickinson, K.M., Freeman, C., 2012. Closing the gap: communicating to community of plants lacking fleshy fruits by storks and gulls. J. Veg. Sci. 32 (1), e12967. change gardening practices in support of native biodiversity in urban private gardens. https://doi.org/10.1111/jvs.12967. Ecol. Soc. 17 (2012), 34–43. https://doi.org/10.5751/ES-04712-170134. Martín-Vélez, V., van Leeuwen, C.H., Sánchez, M.I., Hortas, F., Shamoun-Baranes, J., Thaxter, Vergara, A., Pitart, C., Montalvo, T., Roca, I., Sabaté, S., Hurtado, J.C., Vila, J., 2017. Preva- C.B., Lens, L., Camphuysen, C.J., Green, A.J., 2021. Spatial patterns of weed dispersal by lence of extended-spectrum-β-lactamase-and/or carbapenemase-producing Escherichia wintering gulls within and beyond an agricultural landscape. J. Ecol. 109 (4), coli isolated from yellow-legged gulls from Barcelona, Spain. Antimicrob. Agents 1947–1958. https://doi.org/10.1111/1365-2745.13619. Chemother. 61 (2). https://doi.org/10.1128/AAC.02071-16 e02071-16. McKinney, M.L., Lockwood, J.L., 1999. Biotic homogenization: a few winners replacing many Viana, D.S., Santamaría, L., Figuerola, J., 2016. Optimal methods for fitting probability distri- losers in the next mass extinction. Trends Ecol. Evol. 14, 450–453. https://doi.org/10. butions to propagule retention time in studies of zoochorous dispersal. BMC Ecol. 16 (1), 1016/S0169-5347(99)01679-1. 3. https://doi.org/10.1186/s12898-016-0057-0. Méndez, A., Montalvo, T., Aymí, R., Carmona, M., Figuerola, J., Navarro, J., 2020. Adapting to Vidal, E., Medail, F., Tatoni, T., 1998. Is the yellow-legged gull a superabundant bird species in urban ecosystems: unravelling the foraging ecology of an opportunistic predator living in the Mediterranean? Impact on fauna and flora, conservation measures and research prior- cities. Urban Ecosyst. 23 (5), 1117–1126. https://doi.org/10.1007/s11252-020-00995-3. ities. Biodivers. Conserv. 7 (8), 1013–1026. https://doi.org/10.1023/A:1008805030578. Moreno, R., Jover, L., Munilla, I., Velando, A., Sanpera, C., 2010. A three-isotope approach to Vladimirov, V., Bancheva, S., Delcheva, M., 2015. Solanum elaeagnifolium (Solanaceae), a disentangling the diet of a generalist consumer: the yellow-legged gull in Northwest new alien species for the Bulgarian flora. Fl. Medit 25, 121–125. https://doi.org/10. Spain. Mar. Biol. 157 (3), 545–553. https://doi.org/10.1007/s00227-009-1340-9. 7320/FlMedit25.121. 8 V. Martín-Vélez et al. Science of the Total Environment 823 (2022) 153535 Washburn, B.E., Bernhardt, G.E., Kutschbach-Brohl, L., Chipman, R.B., Francoeur, L.C., 2013. Wongsriphuek, C., Dugger, B.D., Bartuszevige, A.M., 2008. Dispersal of wetland plant seeds Foraging ecology of four gull species at a coastal-urban interface: ecología de forrajeo de by mallards: influence of gut passage on recovery, retention, and germination. Wetlands cuatro especies de gaviota en una interface costera-Urbana. Condor 115 (1), 67–76. 28 (2), 290–299. https://doi.org/10.1672/07-101.1. https://doi.org/10.1525/cond.2013.110185. Yoshikawa, T., Kawakami, K., Masaki, T., 2019. Allometric scaling of seed retention time in Wenny, D.G., Şekercioğlu, Ç.H., Cordeiro, N.J., Rogers, H.S., Kelly, D., 2016. Seed dispersal by seed dispersers and its application to estimation of seed dispersal potentials of theropod fruit-eating birds. Why Birds Matter. University of Chicago Press, pp. 107–146. dinosaurs. Oikos 128 (6), 836–844. https://doi.org/10.1111/oik.05827. 9