Abstract
Pollution is a global concern, increasing rapidly throughout marine and terrestrial ecosystems, and affecting many species. Urbanization enhances waste production, leading to the opening of landfills that constitute a spatially and temporally predictable food source for opportunistic species. Several species of gulls are known to exploit and breed in urban areas, taking advantage of accessible and diverse food resources. The exploitation of anthropogenic food subsidies at sea (e.g. fishery discards), urban sites, and landfills leads to debris ingestion by gulls with potential negative effects. Here we characterize anthropogenic debris ingested by yellow-legged gulls (Larus michahellis) along Portugal, by analysing the content of pellets collected in (1) natural and urban breeding locations, and in (2) urban and landfill resting sites, to assess seasonal patterns in the ingestion of anthropogenic debris. We also relate diet with the presence of anthropogenic debris. Debris materials were found in 28.8% of pellets from breeding locations (natural and urban) and in 89.7% of pellets from resting sites (urban and landfill). Gulls from the most urbanized breeding location exhibited higher levels of ingested materials during the entire breeding cycle, however, gulls from a natural breeding site also ingested high levels of debris during the pre-breeding season. At resting sites, small seasonal differences were detected in the number and mass of debris items ingested, which were both higher during spring and summer. Gulls that typically fed on pelagic fish had significantly less sheet and fragment plastics in their pellets. The presence of certain debris categories in gull pellets was positively related to the presence of some prey items, suggesting that gulls may accidentally ingest debris while foraging at multiple habitats. The quantity of anthropogenic materials ingested by gulls from urban locations and landfills indicates a need for improved waste management.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Acampora H, Lyashevska O, van Franeker JA, O'Connor I (2016) The use of beached bird surveys for marine plastic litter monitoring in Ireland. Mar Environ Res 120:122–129. https://doi.org/10.1016/j.marenvres.2016.08.002
Acampora H, Newton S, O’Connor I (2017) Opportunistic sampling to quantify plastics in the diet of unfledged black legged kittiwakes (Rissa tridactyla), northern fulmars (Fulmarus glacialis) and great cormorants (Phalacrocorax carbo). Mar Pollut Bull 119:171–174. https://doi.org/10.1016/j.marpolbul.2017.04.016
Alonso H, Almeida A, Granadeiro JP, Catry P (2015) Temporal and age-related dietary variations in a large population of yellow-legged gulls Larus michahellis: implications for management and conservation. Eur J Wildl Res 61:819–829. https://doi.org/10.1007/s10344-015-0958-9
Annett CA, Pierotti R (1999) Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297. https://doi.org/10.1890/0012-9658(1999)080[0288:LTROIW]2.0.CO;2
Arizaga J, Aldalur A, Herrero A, Cuadrado JF, Díez E, Crespo A (2014) Foraging distances of a resident yellow-legged gull (Larus michahellis) population in relation to refuse management on a local scale. Eur J Wildl Res 60:171–175. https://doi.org/10.1007/s10344-013-0761-4
Assis CA (2004) Guia para a identificação de algumas famílias de peixes ósseos de Portugal continental, através da morfologia dos seus otólitos sagitta. Câmara Municipal de Cascais
Auman HJ, Meathrel CE, Richardson A (2008) Supersize me: does anthropogenic food change the body condition of silver gulls? A comparison between urbanized and remote, non-urbanized areas. Waterbirds 31:122–126. https://doi.org/10.1675/1524-4695(2008)31[122:SMDAFC]2.0.CO;2
Barnes DKA, Galgani F, Thompson RC, Barlaz M (2009) Accumulation and fragmentation of plastic debris in global environments. Philos Trans R Soc B Biol Sci 364:1985–1998. https://doi.org/10.1098/rstb.2008.0205
Barrett RT, Camphuysen KCJ, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. https://doi.org/10.1093/icesjms/fsm152
Bartumeus F, Giuggioli L, Louzao M, Bretagnolle V, Oro D, Levin SA (2010) Fishery discards impact on seabird movement patterns at regional scales. Curr Biol 20:215–222. https://doi.org/10.1016/j.cub.2009.11.073
Basto MN, Nicastro KR, Tavares AI, McQuaid CD, Casero M, Azevedo F, Zardi GI (2019) Plastic ingestion in aquatic birds in Portugal. Mar Pollut Bull 138:19–24. https://doi.org/10.1016/j.marpolbul.2018.11.024
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Battisti C, Staffieri E, Poeta G, Sorace A, Luiselli L, Amori G (2019) Interactions between anthropogenic litter and birds: a global review with a ‘black-list’ of species. Mar Pollut Bull 138:93–114. https://doi.org/10.1016/j.marpolbul.2018.11.017
Belant JL (1997) Gulls in urban environments: landscape-level management to reduce conflict. Landsc Urban Plan 38:245–258. https://doi.org/10.1016/S0169-2046(97)00037-6
Belant JL, Ickes SK, Seamans TW (1998) Importance of landfills to urban-nesting herring and ring-billed gulls. Landsc Urban Plan 43:11–19. https://doi.org/10.1016/S0169-2046(98)00100-5
Bond AL (2016) Diet changes in breeding herring gulls (Larus argentatus) in Witless Bay, Newfoundland and Labrador, Canada, over 40 years. Waterbirds 39:152–158. https://doi.org/10.1675/063.039.sp115
Bond AL, Jones IL, Williams JC, Byrd GV (2010) Auklet (Charadriiformes: Alcidae, Aethia spp.) chick meals from the Aleutian Islands, Alaska, have a very low incidence of plastic marine debris. Mar Pollut Bull 60:1346–1349. https://doi.org/10.1016/j.marpolbul.2010.05.001
Bueno-Pardo J, Pierce GJ, Cabecinha E, Grilo C, Assis J, Valavanis V, Pita C, Dubert J, Leitão F, Queiroga H (2020) Trends and drivers of marine fish landings in Portugal since its entrance in the European Union. ICES J Mar Sci 77:988–1001. https://doi.org/10.1093/icesjms/fsaa010
Burger J, Gochfeld M (1983) Feeding behavior in laughing gulls: compensatory site selection by young. Condor 85:467–473. https://doi.org/10.2307/1367989
Calado JG, Matos DM, Ramos JA, Moniz F, Ceia FR, Granadeiro JP, Paiva VH (2018) Seasonal and annual differences in the foraging ecology of two gull species breeding in sympatry and their use of fishery discards. J Avian Biol 49:1–12. https://doi.org/10.1111/jav.01463
Calado JG, Paiva VH, Ceia FR, Gomes P, Ramos JA, Velando A (2020) Stable isotopes reveal year-round sexual trophic segregation in four yellow-legged gull colonies. Mar Biol 167:65. https://doi.org/10.1007/s00227-020-3676-0
Ceia FR, Paiva VH, Fidalgo V, Morais L, Baeta A, Crisóstomo P, Mourato E, Garthe S, Marques JC, Ramos JA (2014) Annual and seasonal consistency in the feeding ecology of an opportunistic species, the yellow-legged gull Larus michahellis. Mar Ecol Prog Ser 497:273–284. https://doi.org/10.3354/meps10586
Codina-García M, Militão T, Moreno J, González-Solís J (2013) Plastic debris in Mediterranean seabirds. Mar Pollut Bull 77:220–226. https://doi.org/10.1016/j.marpolbul.2013.10.002
Cristol DA, Akst JG, Curatola MK, Dunlavey EG, Fisk KA, Moody KE (2017) Age-related differences in foraging ability among clam-dropping herring gulls (Larus argentatus). Wilson J Ornithol 129:301–310. https://doi.org/10.1676/15-024.1
Da Cruz NF, Simões P, Marques RC (2012) Economic cost recovery in the recycling of packaging waste: The case of Portugal. J Clean Prod 37:8–18. https://doi.org/10.1016/j.jclepro.2012.05.043
Duhem C, Roche P, Vidal É, Tatoni T (2008) Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands. Popul Ecol 50:91–100. https://doi.org/10.1007/s10144-007-0059-z
Duhem C, Vidal É, Legrand J, Tatoni T (2003a) Opportunistic feeding responses of the yellow-legged gull Larus michahellis to accessibility of refuse dumps. Bird Study 50:61–67. https://doi.org/10.1080/00063650309461291
Duhem C, Vidal É, Roche P, Legrand J (2003b) Island breeding and continental feeding: how are diet patterns in adult yellow-legged gulls influenced by landfill accessibility and breeding stages? Écoscience 10:502–508. https://doi.org/10.1080/11956860.2003.11682798
Duhem C, Vidal É, Roche P, Legrand J (2005) How is the diet of yellow-legged gull chicks influenced by parents’ accessibility to landfills? Waterbirds 28:46–52. https://doi.org/10.1675/1524-4695(2005)028[0046:HITDOY]2.0.CO;2
Duis K, Coors A (2016) Microplastics in the aquatic and terrestrial environment: sources (with a specific focus on personal care products), fate and effects. Environ Sci Eur 28:1–25. https://doi.org/10.1186/s12302-015-0069-y
Egunez A, Zorrozua N, Aldalur A, Herrero A, Arizaga J (2018) Local use of landfills by a yellow-legged gull population suggests distance-dependent resource exploitation. J Avian Biol 49:1–7. https://doi.org/10.1111/jav.01455
English MD, Robertson GJ, Avery-Gomm S, Pirie-Hay D, Roul S, Ryan PC, Wilhelm SI, Mallory ML (2015) Plastic and metal ingestion in three species of coastal waterfowl wintering in Atlantic Canada. Mar Pollut Bull 98:349–353. https://doi.org/10.1016/j.marpolbul.2015.05.063
ERSUC (2020) Perfil ERSUC. Available at: http://ersuc.pt/ersuc/perfil/ (in Portuguese) Visited on 29/06/2020
European Commission (2016) European Union Landfill Directive. Available at: http://ec.europa.eu/environment/waste/landfill_index.htm Visited on 28/06/2020
Fuirst M, Veit RR, Hahn M, Dheilly N, Thorne LH (2018) Effects of urbanization on the foraging ecology and microbiota of the generalist seabird Larus argentatus. PLoS One 13:1–22. https://doi.org/10.1371/journal.pone.0209200
Furtado R, Menezes D, Santos CJ, Catry P (2016) White-faced storm-petrels Pelagodroma marina predated by gulls as biological monitors of plastic pollution in the pelagic subtropical Northeast Atlantic. Mar Pollut Bull 112:117–122. https://doi.org/10.1016/j.marpolbul.2016.08.031
Galgani F, Hanke G, Maes T (2015) Global distribution, composition and abundance of marine litter. In: Gutow L, Klages M (eds) Bergmann M. Springer International Publishing, Marine Anthropogenic Litter, pp 29–56
Gall SC, Thompson RC (2015) The impact of debris on marine life. Mar Pollut Bull 92:170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041
Gilbert NI, Correia RA, Silva JP, Pacheco C, Catry I, Atkinson PW, Gill JA, Franco AMA (2016) Are white storks addicted to junk food? Impacts of landfill use on the movement and behaviour of resident white storks (Ciconia ciconia) from a partially migratory population. Mov Ecol 4:1–13. https://doi.org/10.1186/s40462-016-0070-0
González-Solís J, Oro D, Pedrocchi V, Jover L, Ruiz X (1997) Bias associated with diet samples in Audouin’s gulls. Condor 99:773–779. https://doi.org/10.2307/1370488
Gregory MR (2009) Environmental implications of plastic debris in marine settings-entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos Trans R Soc B Biol Sci 364:2013–2025. https://doi.org/10.1098/rstb.2008.0265
Greig SA, Coulson JC, Monaghan P (1983) Age-related differences in foraging success in the herring gull (Larus argentatus). Anim Behav 31:1237–1243. https://doi.org/10.1016/s0003-3472(83)80030-x
Gyimesi A, Boudewijn TJ, Buijs R-J, Shamoun-Baranes JZ, de Jong JW, Fijn RC, van Horssen PW, Poot MJM (2016) Lesser Black-backed Gulls Larus fuscus thriving on a non-marine diet. Bird Study 63:241–249. https://doi.org/10.1080/00063657.2016.1180341
Hammer S, Nager RG, Johnson PCD, Furness RW, Provencher JF (2016) Plastic debris in great skua (Stercorarius skua) pellets corresponds to seabird prey species. Mar Pollut Bull 103:206–210. https://doi.org/10.1016/j.marpolbul.2015.12.018
Henry PY, Wey G, Balança G (2011) Rubber band ingestion by a rubbish dump dweller, the white stork (Ciconia ciconia). Waterbirds 34:504–508. https://doi.org/10.1675/063.034.0414
Holland ER, Mallory ML, Shutler D (2016) Plastics and other anthropogenic debris in freshwater birds from Canada. Sci Total Environ 571:251–258. https://doi.org/10.1016/j.scitotenv.2016.07.158
Huig N, Buijs RJ, Kleyheeg E (2016) Summer in the city: behaviour of large gulls visiting an urban area during the breeding season. Bird Study 63:214–222. https://doi.org/10.1080/00063657.2016.1159179
INE (2019) Urban waste collected (t) by geographical location and type of recyclable material https://www.ine.pt/xportal/xmain?xpid=INE&xpgid=ine_indicadores&indOcorrCod=0009614&contexto=bd&selTab=tab2 Visited on 28/06/2020
IPMA (2019) Climatological bulletin of April 2018. Available at: http://www.ipma.pt/resources.www/docs/im.publicacoes/edicoes.online/20180514/vzjSWCpQNZMSwEWvWTJz/cli_20180401_20180430_pcl_mm_co_pt.pdf (in Portuguese) Visited on 08/07/2020
Jackman S (2017) Pscl: classes and methods for R developed in the political science computational laboratory. United States Studies Centre, University of Sydney. Sydney, New South Wales, Australia. R package version 1.5.2. URL https://github.com/atahk/pscl/
Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to lipids: Estimating diets of seabirds. Mar Ecol Prog Ser 451:263–284. https://doi.org/10.3354/meps09713
Kühn S, van Franeker JA (2020) Quantitative overview of marine debris ingested by marine megafauna. Mar Pollut Bull 151:110858. https://doi.org/10.1016/j.marpolbul.2019.110858
Kühn S, Rebolledo ELB, van Franeker JA (2015) Deleterious effects of litter on marine life. In: Gutow L, Klages M (eds) Bergmann M. Springer International Publishing, Marine Anthropogenic Litter, pp 75–116
Lavers JL, Bond AL (2016) Ingested plastic as a route for trace metals in Laysan albatross (Phoebastria immutabilis) and Bonin petrel (Pterodroma hypoleuca) from Midway Atoll. Mar Pollut Bull 110:493–500. https://doi.org/10.1016/j.marpolbul.2016.06.001
Lavers JL, Bond AL, Hutton I (2014) Plastic ingestion by flesh-footed shearwaters (Puffinus carneipes): implications for fledgling body condition and the accumulation of plastic-derived chemicals. Environ Pollut 187:124–129. https://doi.org/10.1016/j.envpol.2013.12.020
Lavers JL, Hutton I, Bond AL (2019) Clinical pathology of plastic ingestion in marine birds and relationships with blood chemistry. Environ Sci Technol 53:9224–9231. https://doi.org/10.1021/acs.est.9b02098
Law KL (2017) Plastics in the marine environment. Annu Rev Mar Sci 9:205–229. https://doi.org/10.1146/annurev-marine-010816-060409
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Lindborg VA, Ledbetter JF, Walat JM, Moffett C (2012) Plastic consumption and diet of glaucous-winged gulls (Larus glaucescens). Mar Pollut Bull 64:2351–2356. https://doi.org/10.1016/j.marpolbul.2012.08.020
Lopes CS, Faria JP, Paiva VH, Ramos JA (2020) Characterization of anthropogenic materials on yellow-legged gull (Larus michahellis) nests breeding in natural and urban sites along the coast of Portugal. Environ Sci Pollut Res 27:36954–36969. https://doi.org/10.1007/s11356-020-09651-x
Matos DM, Ramos JA, Calado JG, Ceia FR, Hey J, Paiva VH (2018) How fishing intensity affects the spatial and trophic ecology of two gull species breeding in sympatry. ICES J Mar Sci 75:1949–1964. https://doi.org/10.1093/icesjms/fsy096
Mendes RF, Ramos JA, Paiva VH, Calado JG, Matos DM, Ceia FR (2018) Foraging strategies of a generalist seabird species, the yellow-legged gull, from GPS tracking and stable isotope analyses. Mar Biol 165. https://doi.org/10.1007/s00227-018-3421-0
Méndez A, Montalvo T, Aymí R, Carmona M, Figuerola J, Navarro J (2020) Adapting to urban ecosystems: unravelling the foraging ecology of an opportunistic predator living in cities. Urban Ecosyst 23:1117–1126. https://doi.org/10.1007/s11252-020-00995-3
Morais L, Santos C, Vicente L (1998) Population increase of yellow-legged gulls Larus cachinnans breeding on Berlenga Island (Portugal), 1974-1994. Sula 12:27–37
Nicastro KR, Lo Savio R, McQuaid CD, Madeira P, Valbusa U, Azevedo F, Casero M, Lourenço C, Zardi GI (2018) Plastic ingestion in aquatic-associated bird species in southern Portugal. Mar Pollut Bull 126:413–418. https://doi.org/10.1016/j.marpolbul.2017.11.050
Oro D, Genovart M, Tavecchia G, Fowler MS, Martínez-Abraín A (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514. https://doi.org/10.1111/ele.12187
Parfitt J, Barthel M, Macnaughton S (2010) Food waste within food supply chains: quantification and potential for change to 2050. Philos Trans R Soc B Biol Sci 365:3065–3081. https://doi.org/10.1098/rstb.2010.0126
PlasticsEurope (2019) Plastics Europe – The Facts 2019: an analysis of european plastics production, demand and waste data. Plastics Europe, Brussels
Plaza PI, Lambertucci SA (2017) How are garbage dumps impacting vertebrate demography, heath, and conservation? Glob Ecol Conserv 12:9–20. https://doi.org/10.1016/j.gecco.2017.08.002
PORDATA (2011) https://www.pordata.pt/Subtema/Portugal/Censos+da+População-27 (in Portuguese) Visited on 28/06/2020
Provencher JF, Bond AL, Avery-Gomm S, Borrelle SB, Bravo Rebolledo EL, Hammer S, Kühn S, Lavers JL, Mallory ML, Trevail A, van Franeker JA (2017) Quantifying ingested debris in marine megafauna: a review and recommendations for standardization. Anal Methods 9:1454–1469. https://doi.org/10.1039/c6ay02419j
Provencher JF, Bond AL, Mallory ML (2015) Marine birds and plastic debris in Canada: a national synthesis and a way forward. Environ Rev 23:1–13. https://doi.org/10.1139/er-2014-0039
Provencher JF, Borrelle SB, Bond AL, Lavers JL, van Franeker JA, Kühn S, Hammer S, Avery-Gomm S, Mallory ML (2019) Recommended best practices for plastic and litter ingestion studies in marine birds: collection, processing, and reporting. Facets 4:111–130. https://doi.org/10.1139/facets-2018-0043
Puskic PS, Lavers JL, Adams LR, Grünenwald M, Hutton I, Bond AL (2019) Uncovering the sub-lethal impacts of plastic ingestion by shearwaters using fatty acid analysis. Conserv Physiol 7:1–9. https://doi.org/10.1093/conphys/coz017
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.r-project.org/
Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009) Diet of yellow-legged gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps. J Ornithol 150:265–272. https://doi.org/10.1007/s10336-008-0346-2
Rock P (2005) Urban gulls: Problems and solutions. British Birds 98:338–355
Rodríguez A, Rodríguez B, Carrasco MN (2012) High prevalence of parental delivery of plastic debris in Cory’s shearwaters (Calonectris diomedea). Mar Pollut Bull 64:2219–2223. https://doi.org/10.1016/j.marpolbul.2012.06.011
Ryan PG (1987) The incidence and characteristics of plastic particles ingested by seabirds. Mar Environ Res 23:175–206. https://doi.org/10.1016/0141-1136(87)90028-6
Ryan PG (1988) Intraspecific variation in plastic ingestion by seabirds and the flux of plastic through seabird populations. Condor 90:446–452. https://doi.org/10.2307/1368572
Schmutz JA, Hobson KA (1998) Geographic, temporal, and age-specific variation in diets of glaucous gulls in Western Alaska. Condor 100:119–130. https://doi.org/10.2307/1369903
Seif S, Provencher JF, Avery-Gomm S, Daoust P-Y, Mallory ML, Smith PA (2018) Plastic and non-plastic debris ingestion in three gull species feeding in an urban landfill environment. Arch Environ Contam Toxicol 74:349–360. https://doi.org/10.1007/s00244-017-0492-8
Shealer DA (2002) Foraging behavior and food of seabirds. In: Schreiber EA, Burger J (eds) Biology of Marine Birds. CRC Press, New York, pp 137–177
Skórka P, Wójcik JD, Martyka R (2005) Colonization and population growth of yellow-legged gull Larus cachinnans in southeastern Poland: causes and influence on native species. Ibis 147:471–482. https://doi.org/10.1111/j.1474-919X.2005.00415.x
Sorais M, Mazerolle MJ, Giroux JF, Verreault J (2020) Landfills represent significant atmospheric sources of exposure to halogenated flame retardants for urban-adapted gulls. Environ Int 135:105387. https://doi.org/10.1016/j.envint.2019.105387
Spelt A, Williamson C, Shamoun-Baranes J, Shepard E, Rock P, Windsor S (2019) Habitat use of urban-nesting lesser black-backed gulls during the breeding season. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-46890-6
Tanaka K, Takada H, Yamashita R, Mizukawa K, Fukuwaka M, Watanuki Y (2013) Accumulation of plastic-derived chemicals in tissues of seabirds ingesting marine plastics. Mar Pollut Bull 69:219–222. https://doi.org/10.1016/j.marpolbul.2012.12.010
Thompson RC, Swan SH, Moore CJ, Vom Saal FS (2009) Our plastic age. Philos Trans R Soc B Biol Sci 364:1973–1976. https://doi.org/10.1098/rstb.2009.0054
Tuset V, Lombarte A, Assis CA (2008) Otolith atlas for the western Mediterranean, north and central Eastern Atlantic. Sci Mar 72:7–198. https://doi.org/10.3989/scimar.2008.72s17
UNEP (2016) Marine plastic Debris and microplastics. United Nations Environ Program
van Franeker JA, Blaize C, Danielsen J, Fairclough K, Gollan J, Guse N, Hansen PL, Heubeck M, Jensen JK, Guillou GL, Olsen B, Olsen KO, Pedersen J, Stienen EWM, Turner DM (2011) Monitoring plastic ingestion by the northern fulmar Fulmarus glacialis in the North Sea. Environ Pollut 159:2609–2615. https://doi.org/10.1016/j.envpol.2011.06.008
van Sebille E, Wilcox C, Lebreton L, Maximenko N, Hardesty BD, van Franeker JA, Eriksen M, Siegel D, Galgani F, Law KL (2015) A global inventory of small floating plastic debris. Environ Res Lett 10. https://doi.org/10.1088/1748-9326/10/12/124006
Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth edition. Springer, New York. ISBN 0-387-95457-0. URL http://www.stats.ox.ac.uk/pub/MASS4
Verlis KM, Campbell ML, Wilson SP (2014) Marine debris is selected as nesting material by the brown booby (Sula leucogaster) within the Swain Reefs, Great Barrier Reef, Australia. Mar Pollut Bull 87:180–190. https://doi.org/10.1016/j.marpolbul.2014.07.060
Votier SC, Bearhop S, MacCormick A, Ratcliffe N, Furness RW (2003) Assessing the diet of great skuas, Catharacta skua, using five different techniques. Polar Biol 26:20–26. https://doi.org/10.1007/s00300-002-0446-z
Washburn BE, Bernhardt GE, Kutschbach-Brohl L, Chipman RB, Francoeur LC (2013) Foraging ecology of four gull species at a coastal–urban interface. Condor 115:67–76. https://doi.org/10.1525/cond.2013.110185
Weiser EL, Powell AN (2011) Reduction of garbage in the diet of nonbreeding glaucous gulls corresponding to a change in waste management. Artic 64:220–226 https://www.jstor.org/stable/23025695
Wilcox C, van Sebille E, Hardesty BD (2015) Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proc Natl Acad Sci U S A 112:11899–11904. https://doi.org/10.1073/pnas.1502108112
Witteveen M, Brown M, Ryan PG (2017) Anthropogenic debris in the nests of kelp gulls in South Africa. Mar Pollut Bull 114:699–704. https://doi.org/10.1016/j.marpolbul.2016.10.052
Yorio P, Marinao C, Kasinsky T, Ibarra C, Suárez N (2020) Patterns of plastic ingestion in kelp gull (Larus dominicanus) populations breeding in northern Patagonia, Argentina. Mar Pollut Bull 156:111240. https://doi.org/10.1016/j.marpolbul.2020.111240
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:8 http://www.jstatsoft.org/v27/i08/
Acknowledgments
We are thankful to Câmara Municipal de Peniche (Dr. Rui Venâncio), Fortress of Peniche (Dr. Alda Rechena), Porto La Vie Shopping Centre administration (Dr. Sérgio Queirós), Tribunal da Relação do Porto (Dr. Nuno Ataíde das Neves and Dr. Vera Medeiros), and ERSUC Coimbra (Eng. Rui Fonseca) for giving access to the respective buildings for sample collection. We also acknowledge Ana Quaresma, Rita Soares, Ana Mafalda Marques and Filipe Ceia for the help in the fieldwork. Three anonymous reviewers provided further comments and suggestions, which improved the first draft of the manuscript
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We acknowledge the support of Portuguese national funds provided by FCT–Foundation for Science and Technology, I.P., through the strategic project UIDB/04292/2020 granted to MARE–Marine and Environmental Sciences Centre, and the fellowships SFRH/BD/118862/2016, SFRH/BD/118861/2016, PD/BD/127991/2016 granted to CSL, JPF and JGC, respectively.
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CSL, JAR, and VHP were responsible for the study conception and design. Material preparation and data collection were performed by all authors. Laboratory work was performed by PTV and CSL. The first draft of the manuscript was written by CSL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Lopes, C.S., Paiva, V.H., Vaz, P.T. et al. Ingestion of anthropogenic materials by yellow-legged gulls (Larus michahellis) in natural, urban, and landfill sites along Portugal in relation to diet composition. Environ Sci Pollut Res 28, 19046–19063 (2021). https://doi.org/10.1007/s11356-020-12161-5
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DOI: https://doi.org/10.1007/s11356-020-12161-5