Abstract
Human activities and environmental conditions are the main drivers of ecosystem change. One major alteration near the western Iberian coast has been the collapse of the Atlanto-Iberian sardine Sardina pilchardus stock, with important cascading effects on marine top predators. We investigated the effect of long-term changes in fishery landings, sardine availability and environmental conditions on the diet of the yellow-legged gull Larus michahellis in the northwest coast of Spain, over the last 30 years (1987–2017). Dietary trends of gulls were investigated through the analysis of 5010 pellets that revealed a sharp decline of fish and refuse and a shift to a crustacean-based diet. General additive mixed models showed that both total fish and sardine occurrences in gull pellets were negatively associated with total fishery landings and positively associated with sardine landings, suggesting fish depletion and higher fishing efficiency (i.e. reduced discards) during the study period. The winter North Atlantic Oscillation (NAO) index was also positively related with sardine occurrence in gull pellets, possibly due to low sardine abundance and rough conditions in years with very low NAO values. The refuse decline was most probably caused by the closure of open-air landfills, implemented under the European Union Landfill Directive. Our results suggest that changes in fishing practices and waste disposal were the main factors responsible for the sharp decline of fish and refuse in yellow-legged gull diet.
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12 March 2020
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References
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 61:2010–2011. https://doi.org/10.1007/s10344-015-0958-9
Arcea (2007) Censo de colonias nidificantes de gaivota patiamarela (Larus michahellis) no Parque Nacional marítimo-terrestre illas atlánticas de Galicia: Ano 2006. Servicio Provincial de M.A.N. de Pontevedra, Xunta de Galicia
Arcos JM, Oro D (2002) Significance of nocturnal purse seine fisheries for seabirds: a case study off the Ebro Delta (NW Mediterranean). Mar Biol 141:277–286. https://doi.org/10.1007/s00227-002-0828-3
Arístegui J, Barton ED, Álvarez-Salgado XA, Santos AMP, Figueiras FG, Kifani S, Hernández-León S, Mason E, Machú E, Demarcq H (2009) Sub-regional ecosystem variability in the Canary Current upwelling. Prog Oceanogr 83:33–48. https://doi.org/10.1016/j.pocean.2009.07.031
Barros Á (2015) Censo da poboación reprodutora de corvo mariño cristado (Phalacrocorax aristotelis), gaivota patiamarela (Larus michahellis), gaivota escura (Larus fuscus) e gaivotón (Larus marinus) no Parque Nacional Marítimo-Terrestre das Illas Atlánticas de Galicia: resultados de 2015. Parque Nacional Marítimo-Terrestre das Illas Atlánticas de Galicia. Informe non publicado. Xuño de 2015
Barros Á, Álvarez D, Velando A (2013) Climate influences fledgling sex ratio and sex-specific dispersal in a seabird. PLoS One 8:e71358. https://doi.org/10.1371/journal.pone.0071358
Barton K (2018) MuMIn: multi-model inference. In: R Packag. version 1.42.1. https://cran.r-project.org/package=MuMIn
Begoña SM, Saavedra C, Pierce GJ (2014) Quantifying the predation on sardine and hake by cetaceans in the Atlantic waters of the Iberian Peninsula. Deep Sea Res II Top Stud Oceanogr 106:232–244. https://doi.org/10.1016/j.dsr2.2013.09.040
Bennett JL, Jamieson EG, Ronconi RA, Wong SNP (2017) Variability in egg size and population declines of Herring Gulls in relation to fisheries and climate conditions. Avian Conserv Ecol 12:16. https://doi.org/10.5751/ACE-01118-120216
Bicknell AWJ, Oro D, Camphuysen KCJ, Votier SC (2013) Potential consequences of discard reform for seabird communities. J Appl Ecol 50:649–658. https://doi.org/10.1111/1365-2664.12072
Blight LK, Hobson KA, Kyser TK, Arcese P (2015) Changing gull diet in a changing world: a 150-year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America. Glob Chang Biol 21:1497–1507. https://doi.org/10.1111/gcb.12796
Bodey TW, Jessopp MJ, Votier SC, Gerritsen HD, Cleasby IR, Hamer KC, Patrick SC, Wakefield ED, Bearhop S (2014) Seabird movement reveals the ecological footprint of fishing vessels. Curr Biol 24:R514–R515. https://doi.org/10.1016/j.cub.2014.04.041
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
Borges MF, Santos AMP, Crato N, Mendes H, Mota B (2003) Sardine regime shifts off Portugal: a time series analysis of catches and wind conditions. Sci Mar 67:235–244. https://doi.org/10.3989/scimar.2003.67s1235
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York
Cairns DK (1988) Seabirds as indicators of marine food supplies. Biol Oceanogr 5:261–271. https://doi.org/10.1080/01965581.1987.10749517
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
Cardona L, Martínez-Iñigo L, Mateo R, González-Solís J (2015) The role of sardine as prey for pelagic predators in the western Mediterranean Sea assessed using stable isotopes and fatty acids. Mar Ecol Prog Ser 531:1–14. https://doi.org/10.3354/meps11353
Carrera P, Porteiro C (2003) Stock dynamic of the Iberian sardine (Sardina pilchardus, W.) and its implication on the fishery off Galicia (NW Spain). Sci Mar 67:245–258. https://doi.org/10.3989/scimar.2003.67s1245
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
Cubaynes S, Doherty PF, Schreiber EA, Gimenez O (2011) To breed or not to breed: a seabird’s response to extreme climatic events. Biol Lett 7:303–306. https://doi.org/10.1098/rsbl.2010.0778
Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Osterblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706. https://doi.org/10.1126/science.1183640
Duhem C, Vidal E, Legrand J, Tatoni T (2003) Opportunistic feeding responses of the yellow-legged Gull Larus michahellis to accessibility of refuse dumps. Bird Stud 50:61–67. https://doi.org/10.1080/00063650309461291
European Commission (1999) European council directive 1999/31/ EC of 26 April 1999 on the landfill of waste. Off J Eur Communities L182:1–19
European Union (2013) Regulation (EU) No 1380/2013 of the European Parliament and of the Council of 11 December 2013 on the Common Fisheries Policy, amending Council Regulations (EC) No 1954/2003 and (EC) No 1224/2009 and repealing Council Regulations (EC) No 2371/2002 and (EC) No 639/2004 and Council Decision 2004/585/EC. Off J Eur Union L354:22–61
European Union (2015) R Regulation (EU) 2015/812 of the European Parliament and of the Council of 20 May 2015 amending Council Regulations (EC) No 850/98, (EC) No 2187/2005, (EC) No 1967/2006, (EC) No 1098/2007, (EC) No 254/2002, (EC) No 2347/ 2002 and (EC) No 1224/2009, and Regulations (EU) No 1379/ 2013 and (EU) No 1380/2013 of the European Parliament and of the Council, as regards the landing obligation, and repealing Council Regulation (EC) No 1434/98. Off J Eur Union L133:1–20
Fagundes AI, Ramos JA, Ramos U, Medeiros R, Paiva VH (2016) Breeding biology of a winter-breeding procellariiform in the North Atlantic, the Macaronesian shearwater Puffinus lherminieri baroli. Zoology 119:421–429. https://doi.org/10.1016/j.zool.2016.05.014
Fariña AC, Freire J, González-Gurriarán E (1997) Megabenthic decapod crustacean assemblages on the Galician continental shelf and upper slope (north-west Spain). Mar Biol 127:419–434. https://doi.org/10.1007/s002270050029
Feijó D, Marçalo A, Bento T, Barra J, Marujo D, Correia M, Silva A (2018) Trends in the activity pattern, fishing yields, catch and landing composition between 2009 and 2013 from onboard observations in the Portuguese purse seine fleet. Reg Stud Mar Sci 23:97–106. https://doi.org/10.1016/j.rsma.2017.12.007
Foster S, Swann RL, Furness RW (2017) Can changes in fishery landings explain long-term population trends in gulls? Bird Stud 64:90–97. https://doi.org/10.1080/00063657.2016.1274287
Furness RW, Camphuysen KCJ (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54:726–737. https://doi.org/10.1006/jmsc.1997.0243
Furness RW, Tasker ML (2000) Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Mar Ecol Prog Ser 202:253–264. https://doi.org/10.3354/meps202253
Garrido S, Silva A, Marques V, Figueiredo I, Bryère P, Mangin A, Santos AMP (2017) Temperature and food-mediated variability of European Atlantic sardine recruitment. Prog Oceanogr 159:267–275. https://doi.org/10.1016/j.pocean.2017.10.006
Garrido S, Silva A, Pastor J, Dominguez R, Silva A, Santos A (2015) Trophic ecology of pelagic fish species off the Iberian coast: diet overlap, cannibalism and intraguild predation. Mar Ecol Prog Ser 539:271–285. https://doi.org/10.3354/meps11506
Garthe S, Camphuysen K C. J.), Furness RW (1996) Amounts of discards by commercial fisheries and their significance as food for seabirds in the North Sea. Mar Ecol Prog Ser 136:1–11. https://doi.org/10.3354/meps136001
Gomes MC, Serrão E, de Borges MF (2001) Spatial patterns of groundfish assemblages on the continental shelf of Portugal. ICES J Mar Sci 58:633–647. https://doi.org/10.1006/jmsc.2001.1052
Goyert HF, Garton EO, Poe AJ (2018) Effects of climate change and environmental variability on the carrying capacity of Alaskan seabird populations. Auk 135:975–991. https://doi.org/10.1642/AUK-18-37.1
Grecian WJ, Witt MJ, Attrill MJ, Bearhop S, Becker PH, Egevang C, Furness RW, Godley BJ, González-Solís J, Grémillet D, Kopp M, Lescroël A, Matthiopoulos J, Patrick SC, Peter H-UU, Phillips RA, Stenhouse IJ, Votier SC (2016) Seabird diversity hotspot linked to ocean productivity in the Canary Current Large Marine Ecosystem. Biol Lett 12:20160024. https://doi.org/10.1098/rsbl.2016.0024
Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S, Crawford RJM, Ryan PG (2008) A junk-food hypothesis for gannets feeding on fishery waste. Proc R Soc B Biol Sci 275:1149–1156. https://doi.org/10.1098/rspb.2007.1763
Grémillet D, Ponchon A, Paleczny M, Palomares M-LD, Karpouzi V, Pauly D (2018) Persisting worldwide seabird-fishery competition despite seabird community decline. Curr Biol 28:4009–4013.e2. https://doi.org/10.1016/j.cub.2018.10.051
Guillemette M, Grégoire F, Bouillet D, Rail J-F, Bolduc F, Caron A, Pelletier D (2018) Breeding failure of seabirds in relation to fish depletion: is there one universal threshold of food abundance? Mar Ecol Prog Ser 587:235–245. https://doi.org/10.3354/meps12442
Guisande C, Cabanas JM, Vergara AR, Riveiro I (2001) Effect of climate on recruitment success of Atlantic Iberian sardine Sardina pilchardus. Mar Ecol Prog Ser 223:243–250. https://doi.org/10.3354/meps223243
Guisande C, Vergara AR, Riveiro I, Cabanas JM (2004) Climate change and abundance of the Atlantic-Iberian sardine (Sardina pilchardus). Fish Oceanogr 13:91–101. https://doi.org/10.1046/j.1365-2419.2003.00276.x
Gulka J, Carvalho PC, Jenkins E, Johnson K, Maynard L, Davoren GK (2017) Dietary niche shifts of multiple marine predators under varying prey availability on the Northeast Newfoundland coast. Front Mar Sci 4:324. https://doi.org/10.3389/fmars.2017.00324
Gwiazda R (2004) Fish in a diet of cormorant and yellow-legged gull breeding near fish-ponds (upper Vistula river valley, southern Poland) – preliminary study. Acta Zool Cracov 47:17–26
Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMPP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. https://doi.org/10.1126/science.1149345
Harley CDGG, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJBB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL, Hughes AR, Hultgren KM, Miner BG, Sorte CJBB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241. https://doi.org/10.1111/j.1461-0248.2005.00871.x
Howells RJ, Burthe SJ, Green JA, Harris MP, Newell MA, Butler A, Johns DG, Carnell EJ, Wanless S, Daunt F, Daunt F (2017) From days to decades: short- and long-term variation in environmental conditions affect offspring diet composition of a marine top predator. Mar Ecol Prog Ser 583:227–242. https://doi.org/10.3354/meps12343
Howells RJ, Burthe SJ, Green JA, Harris MP, Newell MA, Butler A, Wanless S, Daunt F (2018) Pronounced long-term trends in the diet composition of the European shag Phalacrocorax aristotelis. Mar Biol 165:188. https://doi.org/10.1007/s00227-018-3433-9
Hurrell JW (1995) Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitation. Science 269:676–679. https://doi.org/10.1126/science.269.5224.676
Hurrell JW, Kushnir Y, Ottersen G, Visbeck M (2003) An overview of the North Atlantic Oscillation. In: Geophysical Monograph Series. pp 1–35
Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:768–768. https://doi.org/10.1111/ele.12270
ICES (2017) ICES advice on fishing opportunities, catch and effort of sardine (Sardina pilchardus) in divisions 8.c and 9.a (Cantabrian Sea and Atlantic Iberian waters). 2016:7. https://doi.org/10.17895/ices.pub.3068
IPCC (2014) Climate change 2014: synthesis report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, Switzerland, p 151
Kowalczyk ND, Chiaradia A, Preston TJ, Reina RD (2014) Linking dietary shifts and reproductive failure in seabirds: a stable isotope approach. Funct Ecol 28:755–765. https://doi.org/10.1111/1365-2435.12216
Kroodsma DA, Mayorga J, Hochberg T, Miller NA, Boerder K, Ferretti F, Wilson A, Bergman B, White TD, Block BA, Woods P, Sullivan B, Costello C, Worm B (2018) Tracking the global footprint of fisheries. Science 359:904–908. https://doi.org/10.1126/science.aao5646
Leitão F, Alms V, Erzini K (2014) A multi-model approach to evaluate the role of environmental variability and fishing pressure in sardine fisheries. J Mar Syst 139:128–138. https://doi.org/10.1016/j.jmarsys.2014.05.013
López H, Pérez AJ, Rumeu B, Nogales M (2016) Trophic strategies of yellow-legged Gull Larus michahellis on oceanic islands surrounded by deep waters. Bird Stud 63:337–345. https://doi.org/10.1080/00063657.2016.1194804
Louzão M, Afán I, Santos M, Brereton T (2015) The role of climate and food availability on driving decadal abundance patterns of highly migratory pelagic predators in the Bay of Biscay. Front Ecol Evol 3:90. https://doi.org/10.3389/fevo.2015.00090
Luczak C, Beaugrand G, Lindley JA, Dewarumez J-M, Dubois PJ, Kirby RR (2012) North Sea ecosystem change from swimming crabs to seagulls. Biol Lett 8:821–824. https://doi.org/10.1098/rsbl.2012.0474
MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609. https://doi.org/10.1086/282454
Marçalo A, Nicolau L, Giménez J, Ferreira M, Santos J, Araújo H, Silva A, Vingada J, Pierce GJ (2018) Feeding ecology of the common dolphin (Delphinus delphis) in Western Iberian waters: has the decline in sardine (Sardina pilchardus) affected dolphin diet? Mar Biol 165:44–16. https://doi.org/10.1007/s00227-018-3285-3
Martins MM, Skagen D, Marques V, Zwolinski J, Silva A (2013) Changes in the abundance and spatial distribution of the Atlantic chub mackerel (Scomber colias) in the pelagic ecosystem and fisheries off Portugal. Sci Mar 77:551–563. https://doi.org/10.3989/scimar.03861.07B
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
Maxwell SM, Hazen EL, Bograd SJ, Halpern BS, Breed GA, Nickel B, Teutschel NM, Crowder LB, Benson S, Dutton PH, Bailey H, Kappes MA, Kuhn CE, Weise MJ, Mate B, Shaffer SA, Hassrick JL, Henry RW, Irvine L, McDonald BI, Robinson PW, Block BA, Costa DP (2013) Cumulative human impacts on marine predators. Nat Commun 4:2688. https://doi.org/10.1038/ncomms3688
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 165:168–114. https://doi.org/10.1007/s00227-018-3421-0
Montevecchi WA, Myers A (1996) Dietary changes of seabirds indicate shifts in pelagic food webs. Sarsia 80:313–322. https://doi.org/10.1080/00364827.1996.10413606
Montevecchi WA, Myers RA (1997) Centurial and decadal oceanographic influences on changes in northern gannet populations and diets in the north-west Atlantic: implications for climate change. ICES J Mar Sci 54:608–614. https://doi.org/10.1006/jmsc.1997.0265
Moreno R, Jover L, Munilla I, Velando A, Sanpera C (2010) A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Mar Biol 157:545–553. https://doi.org/10.1007/s00227-009-1340-9
Morlini I (2006) On multicollinearity and concurvity in some nonlinear multivariate models. Stat Methods Appl 15:3–26. https://doi.org/10.1007/s10260-006-0005-9
Mouriño J, Arcos F, Salvadores R, Sandoval A, Vidal C (2003) Status of the Balearic shearwater (Puffinus mauretanicus) on the Galician coast (NW Iberian Peninsula). Sci Mar 67:135–142. https://doi.org/10.3989/scimar.2003.67s2135
Munilla I (1997) Henslow’s swimming crab (Polybius henslowii) as an important food for yellow-legged gulls (Larus cachinnans) in NW Spain. ICES J Mar Sci 54:631–634. https://doi.org/10.1006/jmsc.1997.0249
Neves VC, Murdoch N, Furness RW (2006) Population status and diet of the yellow-legged gull in the Azores. Life Mar Sci 23:59–73
Oro D, Hérnandez N, Jover L, Genovart M (2014) From recruitment to senescence: food shapes the age-dependent pattern of breeding performance in a long-lived bird. Ecology 95:446–457. https://doi.org/10.1890/13-0331.1
Oro D, Ruiz X (1997) Exploitation of trawler discards by breeding seabirds in the north-western Mediterranean: differences between the Ebro Delta and the Balearic Islands areas. ICES J Mar Sci 54:695–707. https://doi.org/10.1006/jmsc.1997.0246
Osborn TJ (2011) Winter 2009/2010 temperatures and a record-breaking North Atlantic Oscillation index. Weather 66:19–21. https://doi.org/10.1002/wea.660
Paiva VH, Geraldes P, Marques V, Rodríguez R, Garthe S, Ramos JA (2013a) Effects of environmental variability on different trophic levels of the North Atlantic food web. Mar Ecol Prog Ser 477:15–28. https://doi.org/10.3354/meps10180
Paiva VH, Geraldes P, Ramirez I, Werner AC, Garthe S, Ramos JA (2013b) Overcoming difficult times: the behavioural resilience of a marine predator when facing environmental stochasticity. Mar Ecol Prog Ser 486:277–288. https://doi.org/10.3354/meps10332
Pardo D, Jenouvrier S, Weimerskirch H, Barbraud C (2017) Effect of extreme sea surface temperature events on the demography of an age-structured albatross population. Philos Trans R Soc B Biol Sci 372:20160143. https://doi.org/10.1098/rstb.2016.0143
Patrick SC, Bearhop S, Bodey TW, Grecian WJ, Hamer KC, Lee J, Votier SC (2015) Individual seabirds show consistent foraging strategies in response to predictable fisheries discards. J Avian Biol 46:001–010. https://doi.org/10.1111/jav.00660
Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F, Pauly FT Jr (1998) Fishing down marine food webs. Science 279:860–863. https://doi.org/10.1126/science.279.5352.860
Payo-Payo A, Genovart M, Bertolero A, Pradel R, Oro D (2016) Consecutive cohort effects driven by density-dependence and climate influence early-life survival in a long-lived bird. Proc R Soc B Biol Sci 283:20153042. https://doi.org/10.1098/rspb.2015.3042
Pedro PI, Ramos JA, Neves VC, Paiva VH (2013) Past and present trophic position and decadal changes in diet of yellow-legged Gull in the Azores Archipelago, NE Atlantic. Eur J Wildl Res 59:833–845. https://doi.org/10.1007/s10344-013-0737-4
Pérez C, Barros Á, Velando A, Munilla I, López Á, Velando A, Munilla I (2012) Seguimento das poboacións reprodutoras de corvo mariño e gaivota patimarela do Parque Nacional das illas Atlánticas de Galicia. Informe de Ecoplanin, Xestión e Información Ambiental S.L
Peterson SH, Ackerman JT, Eagles-Smith CA, Herzog MP, Hartman CA (2018) Prey fish returned to Forster’s tern colonies suggest spatial and temporal differences in fish composition and availability. PLoS One 13:e0193430. https://doi.org/10.1371/journal.pone.0193430
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.r-project.org/
Ramírez F, Gutiérrez-Expósito C, Afán I, Giménez J, De Stephanis R, Forero MG (2015) Human influence on gull non-breeding distribution: potential consequences of changes in fishing practices. Mar Ecol Prog Ser 527:221–232. https://doi.org/10.3354/meps11282
Ramos JA, Isabel Fagundes A, Xavier JC, Fidalgo V, Ceia FR, Medeiros R, Paiva VH (2015) A switch in the Atlantic Oscillation correlates with inter-annual changes in foraging location and food habits of Macaronesian shearwaters (Puffinus baroli) nesting on two islands of the sub-tropical Atlantic Ocean. Deep Sea Res I Oceanogr Res Pap 104:60–71. https://doi.org/10.1016/j.dsr.2015.07.001
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
Real E, Oro D, Martínez-Abraín A, Igual JM, Bertolero A, Bosch M, Tavecchia G (2017) Predictable anthropogenic food subsidies, density-dependence and socio-economic factors influence breeding investment in a generalist seabird. J Avian Biol 48:1462–1470. https://doi.org/10.1111/jav.01454
Reynolds RW, Rayner NA, Smith TM, Stokes DC, Wang W (2002) An improved in situ and satellite SST analysis for climate. J Clim 15:1609–1625. https://doi.org/10.1175/1520-0442(2002)015<1609:AIISAS>2.0.CO;2
Riordan J, Birkhead T (2018) Changes in the diet composition of common guillemot Uria aalge chicks on Skomer Island, Wales, between 1973 and 2017. Ibis (Lond 1859) 160:470–474. https://doi.org/10.1111/ibi.12570
Ronconi RA, Steenweg RJ, Taylor PD, Mallory ML (2014) Gull diets reveal dietary partitioning, influences of isotopic signatures on body condition, and ecosystem changes at a remote colony. Mar Ecol Prog Ser 514:247–261. https://doi.org/10.3354/meps10980
Rosa R, Gonzalez L, Broitman BR, Garrido S, Santos AMP, Nunes ML (2010) Bioenergetics of small pelagic fishes in upwelling systems: relationship between fish condition, coastal ecosystem dynamics and fisheries. Mar Ecol Prog Ser 410:205–218. https://doi.org/10.3354/meps08635
Santos AMP, Chícharo A, Dos Santos A, Moita T, Oliveira PB, Peliz Á, Ré P (2007) Physical–biological interactions in the life history of small pelagic fish in the Western Iberia Upwelling Ecosystem. Prog Oceanogr 74:192–209. https://doi.org/10.1016/j.pocean.2007.04.008
Santos AMP, Kazmin AS, Peliz Á (2005) Decadal changes in the canary upwelling system as revealed by satellite observations: their impact on productivity. J Mar Res 63:359–379. https://doi.org/10.1357/0022240053693671
Santos AMP, Nieblas A-E, Verley P, Teles-Machado A, Bonhommeau S, Lett C, Garrido S, Peliz A (2018) Sardine (Sardina pilchardus) larval dispersal in the Iberian upwelling system, using coupled biophysical techniques. Prog Oceanogr 162:83–97. https://doi.org/10.1016/j.pocean.2018.02.011
Santos MB, González-Quirós R, Riveiro I, Cabanas JM, Porteiro C, Pierce GJ (2012) Cycles, trends, and residual variation in the Iberian sardine (Sardina pilchardus) recruitment series and their relationship with the environment. ICES J Mar Sci 69:739–750. https://doi.org/10.1093/icesjms/fsr186
Signa G, Cartes JE, Solé M, Serrano A, Sánchez F (2008) Trophic ecology of the swimming crab Polybius henslowii Leach, 1820 in Galician and Cantabrian seas: influences of natural variability and the Prestige oil spill. Cont Shelf Res 28:2659–2667. https://doi.org/10.1016/j.csr.2008.08.008
Silva A, Moreno A, Riveiro I, Santos B, Pita C, Garcia, Rodrigues Joao Villasante S, Pawlowski L, Duhamel E (2015) Research for Pech Committee - sardine fisheries: resource assessment and social and economic situation. Cambridge University Press, Cambridge
Silva A, Skagen DW, Uriarte A, Masse J, Santos MB, Marques V, Carrera P, Beillois P, Pestana G, Porteiro C, Stratoudakis Y (2009) Geographic variability of sardine dynamics in the Iberian Biscay region. ICES J Mar Sci 66:495–508. https://doi.org/10.1093/icesjms/fsn225
Sousa P, Azevedo M, Gomes MC (2005) Demersal assemblages off Portugal: mapping, seasonal, and temporal patterns. Fish Res 75:120–137. https://doi.org/10.1016/j.fishres.2005.03.012
Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Chan K, Lima M (2002) Ecological effects of climate fluctuations. Science 297:1292–1296. https://doi.org/10.1126/science.1071281
Stenseth NC, Ottersen G, Hurrell JW, Mysterud A, Lima M, Chan K-S, Yoccoz NG, Adlandsvik B (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proc Biol Sci 270:2087–2096. https://doi.org/10.1098/rspb.2003.2415
Stratoudakis Y, Marçalo A (2002) Sardine slipping during purse-seining off northern Portugal. ICES J Mar Sci 59:1256–1262. https://doi.org/10.1006/jmsc.2002.1314
Sydeman WJ, Poloczanska E, Reed TE, Thompson SA (2015) Climate change and marine vertebrates. Science 350:772–777. https://doi.org/10.1126/science.aac9874
Tenore KR, Alonso-Noval M, Alvarez-Ossorio M, Atkinson LP, Cabanas JM, Cal RM, Campos HJ, Castillejo F, Chesney EJ, Gonzalez N, Hanson RB, McClain CR, Miranda A, Roman MR, Sanchez J, Santiago G, Valdes L, Varela M, Yoder J (1995) Fisheries and oceanography off Galicia, NW Spain: mesoscale spatial and temporal changes in physical processes and resultant patterns of biological productivity. J Geophys Res Ocean 100:10943–10966. https://doi.org/10.1029/95JC00529
Tremblay Y, Bertrand S, Henry R, Kappes M, Costa D, Shaffer S (2009) Analytical approaches to investigating seabird–environment interactions: a review. Mar Ecol Prog Ser 391:153–163. https://doi.org/10.3354/meps08146
Valeiras J (2003) Attendance of scavenging seabirds at trawler discards off Galicia, Spain. Sci Mar 67:77–82. https://doi.org/10.3989/scimar.2003.67s277
van Donk S, Camphuysen KCJ, Shamoun-Baranes J, van der Meer J (2017) The most common diet results in low reproduction in a generalist seabird. Ecol Evol 7:4620–4629. https://doi.org/10.1002/ece3.3018
Veiga-Malta T, Szalaj D, Angélico M, Azevedo M, Farias I, Garrido S, Lourenço S, Marçalo A, Marques V, Moreno A, Oliveira P, Paiva V, Prista N, Silva C, Sobrinho-Gonçalves L, Vingada J, Silva A (2019) First representation of the trophic structure and functioning of the Portuguese continental shelf ecosystem: insights into the role of sardine. Mar Ecol Prog Ser 617–618:323–340. https://doi.org/10.3354/meps12724
Vihtakari M, Welcker J, Moe B, Chastel O, Tartu S, Hop H, Bech C, Descamps S, Gabrielsen GW (2018) Black-legged kittiwakes as messengers of Atlantification in the Arctic. Sci Rep 8:1–23. https://doi.org/10.1038/s41598-017-19118-8
Votier SC, Bearhop S, Fyfe R, Furness RW (2008) Temporal and spatial variation in the diet of a marine top predator-links with commercial fisheries. Mar Ecol Prog Ser 367:223–232. https://doi.org/10.3354/meps07621
Wagner EL, Boersma PD (2011) Effects of fisheries on seabird community ecology. Rev Fish Sci 19:157–167. https://doi.org/10.1080/10641262.2011.562568
Wood SN (2017) Generalized additive models: an introduction with R (2nd edition). Chapman and Hall/CRC, Boca Raton
Wu L, Liu X, Fu P, Xu L, Li D, Li Y (2017) Dietary change in seabirds on Guangjin Island, South China Sea, over the past 1200 years inferred from stable isotope analysis. The Holocene 27:331–338. https://doi.org/10.1177/0959683616660163
Zeller D, Cashion T, Palomares M, Pauly D (2018) Global marine fisheries discards: a synthesis of reconstructed data. Fish Fish 19:30–39. https://doi.org/10.1111/faf.12233
Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York
Zuur AF, Ieno EN, Walker N, Saveliev A a., Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
Dr. Jose Guitián and the staff of the National Park of the Atlantic Islands of Galicia are acknowledged for the help and support during fieldwork all over these years.
Funding
We received the support of Portuguese national funds provided by ‘Fundação para a Ciência e a Tecnologia, I.P.’ (FCT), through the strategic project UIDB/04292/2020 granted to MARE and the fellowships PD/BD/127991/2016 and SFRH/BPD/85024/2012 granted to JGC and VHP, respectively.
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Calado, J.G., Paiva, V.H., Ramos, J.A. et al. Anthropogenic food resources, sardine decline and environmental conditions have triggered a dietary shift of an opportunistic seabird over the last 30 years on the northwest coast of Spain. Reg Environ Change 20, 10 (2020). https://doi.org/10.1007/s10113-020-01609-6
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DOI: https://doi.org/10.1007/s10113-020-01609-6