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Individual specialization in the foraging and feeding strategies of seabirds: a review

  • Review, concept, and synthesis
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Abstract

Trophic relationships are a central theme in ecology and play a crucial role in the survival of organisms, because the availability of food resources varies over time and space. Until recently, most ecological studies treated conspecific individuals as ecologically equivalent, but intra-specific variation in individual foraging and feeding strategies can be large. Studies documenting the occurrence of individual specialization in seabirds (n = 94) increased substantially since the year 2000, and rapid and significant advances are being made since then. This review summarizes existing knowledge within this subject, examines the relative incidence of individual specialization and investigates the possible ecological implications of individual specialization in seabirds. Our results show that, to date, the incidence of individual specialization is documented in around 12 % of the total extant seabird species although some studies (n = 12) did not find evidences of individual specialization in the foraging and feeding strategies of some seabird populations. Most studies were conducted at higher latitudes, leading to a lack of knowledge on the incidence of this trait in tropical seabird populations. Results suggest that the incidence of individual specialization may be potentially widespread within seabirds, but may fluctuate spatio-temporally among/within species and populations due to the frequency of specialists, predictability of resources or environmental conditions. This study supports the hypothesis that individual specialization may have important ecological consequences at both individual and population levels, such as implications in breeding performance or in intra-specific competition and, consequently, a high impact on ecological processes and foraging dynamics. Further investigation is required to identify the mechanisms that generate individual specialization and its ecological implications at both population and individual levels.

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References

  • Anderson OR, Phillips RA, Shore RF, McGill RA, McDonald RA, Bearhop S (2009) Diet, individual specialisation and breeding of brown skuas (Catharacta antarctica lonnbergi): an investigation using stable isotopes. Polar Biol 32:27–33. doi:10.1007/s00300-008-0498-9

    Article  Google Scholar 

  • Annett C, Pierotti R (1999) Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297

    Article  Google Scholar 

  • Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958. doi:10.1111/j.1461-0248.2011.01662.x

    Article  Google Scholar 

  • Arizaga J, Jover L, Aldalur A, Cuadrado JF, Herrero A, Sanpera C (2013) Trophic ecology of a resident yellow-legged gull (Larus michahellis) population in the Bay of Biscay. Mar Environ Res 87–88:19–25

    Article  CAS  Google Scholar 

  • Baylis AMM, Orben RA, Pistorius P, Brickle P, Staniland I, Ratcliffe N (2015) Winter foraging site fidelity of king penguins breeding at the Falkland Islands. Mar Biol 162:99–110. doi:10.1007/s00227-014-2561-0

    Article  Google Scholar 

  • Bearhop S, Phillips R, Thompson D, Waldron S, Furness R (2000) Variability in mercury concentrations of great skuas Catharacta skua: the influence of colony, diet and trophic status inferred from stable isotope signatures. Mar Ecol Prog Ser 195:261–268. doi:10.3354/meps195261

    Article  CAS  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. doi:10.1111/j.0021-8790.2004.00861.x

    Article  Google Scholar 

  • Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164. doi:10.3354/meps311157

    Article  Google Scholar 

  • Bech C, Langseth I, Gabrielsen GW (1999) Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla. Proc R Soc B Biol Sci 266:2161–2167. doi:10.1098/rspb.1999.0903

    Article  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. doi:10.1016/j.anbehav.2008.12.022

    Article  Google Scholar 

  • BirdLife International (2014) The birdLife checklist of the birds of the world: version 7. http://www.birdlife.org/datazone/userfiles/file/Species/Taxonomy/BirdLife_Checklist_Version_70.zip

  • Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659. doi:10.1016/j.tree.2010.08.003

    Article  Google Scholar 

  • Bolnick DI (2004) Can intraspecific competition drive disruptive selection? an experimental test in natural populations of sticklebacks. Evolution 58:608–618

    Article  Google Scholar 

  • Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanbäck R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941. doi:10.1890/0012-9658

    Article  Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi:10.1086/343878

    Article  Google Scholar 

  • Burrows MT, Hughes RN (1991) Variation in foraging behavior among individuals and populations of dog whelks, Nucella lapillus: natural constraints on energy intake. J Anim Ecol 60:497–514

    Article  Google Scholar 

  • Carboneras C, Tavecchia G, Genovart M, Requena S, Olivé M, Oro D (2013) Inferring geographic origin, population structure and migration routes of a wintering population of Mediterranean gulls from resightings data. Popul Ecol 55:343–351. doi:10.1007/s10144-013-0362-9

    Article  Google Scholar 

  • Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653. doi:10.1111/j.0030-1299.2008.16513.x

    Article  Google Scholar 

  • Carneiro APB, Manica A, Phillips RA (2014) Foraging behaviour and habitat use by brown skuas Stercorarius lonnbergi breeding at South Georgia. Mar Biol 161:1755–1764. doi:10.1007/s00227-014-2457-z

    Article  Google Scholar 

  • Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bioindicators of mercury contamination in the Southern Ocean: birds from the Kerguelen Islands as a case study. Sci Total Environ 454–455:141–148. doi:10.1016/j.scitotenv.2013.02.060

    Article  CAS  Google Scholar 

  • Catry P, Dias MP, Phillips RA, Granadeiro JP (2011) Different means to the same end: long-distance migrant seabirds from two colonies differ in behaviour, despite common wintering grounds. PLoS ONE 6:e26079. doi:10.1371/journal.pone.0026079

    Article  CAS  Google Scholar 

  • Catry T, Alves JA, Gill JA, Gunnarsson TG, Granadeiro JP (2014) Individual specialization in a shorebird population with narrow foraging niche. Acta Oecol 56:56–65. doi:10.1016/j.actao.2014.03.001

    Article  Google Scholar 

  • Ceia FR, Phillips RA, Ramos JA, Cherel Y, Vieira RP, Richard P, Xavier JC (2012) Short- and long-term consistency in the foraging niche of wandering albatrosses. Mar Biol 159:1581–1591. doi:10.1007/s00227-012-1946-1

    Article  Google Scholar 

  • Ceia FR, Paiva VH, Fidalgo V, Morais L, Baeta A, Crisóstomo P, Mourato E, Garthe S, Marques JC, Ramos JA (2014a) 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. doi:10.3354/meps10586

    Article  Google Scholar 

  • Ceia FR, Paiva VH, Garthe S, Marques JC, Ramos JA (2014b) Can variations in the spatial distribution at sea and isotopic niche width be associated with consistency in the isotopic niche of a pelagic seabird species? Mar Biol 161:1861–1872. doi:10.1007/s00227-014-2468-9

    Article  Google Scholar 

  • Ceia FR, Paiva VH, Ceia RS, Hervías S, Garthe S, Marques JC, Ramos JA (2015) Spatial foraging segregation by close neighbours in a wide-ranging seabird. Oecologia 177:431–440. doi:10.1007/s00442-014-3109-1

    Article  Google Scholar 

  • Cherel Y, Phillips RA, Hobson KA, McGill R (2006) Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds. Biol Lett 2:301–303. doi:10.1098/rsbl.2006.0445

    Article  CAS  Google Scholar 

  • Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76:826–836. doi:10.1111/j.1365-2656.2007.01238.x

    Article  Google Scholar 

  • Cook TR, Cherel Y, Tremblay Y (2006) Foraging tactics of chick-rearing Crozet shags: individuals display repetitive activity and diving patterns over time. Polar Biol 29:562–569. doi:10.1007/s00300-005-0089-y

    Article  Google Scholar 

  • Croxall JP, Silk JR, Phillips RA, Afanasyev V, Briggs DR (2005) Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science 307:249–250. doi:10.1126/science.1106042

    Article  CAS  Google Scholar 

  • Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34. doi:10.1017/S0959270912000020

    Article  Google Scholar 

  • Dias MP, Granadeiro JP, Phillips RA, Alonso H, Catry P (2011) Breaking the routine: individual Cory’s shearwaters shift winter destinations between hemispheres and across ocean basins. Proc R Soc B 2:1786–1793. doi:10.1098/rspb.2010.2114

    Article  Google Scholar 

  • Dias MP, Granadeiro JP, Catry P (2013) Individual variability in the migratory path and stopovers of a long-distance pelagic migrant. Anim Behav 86:359–364. doi:10.1016/j.anbehav.2013.05.026

    Article  Google Scholar 

  • Elliott K, Woo K, Gaston A, Benvenuti S, Dall’Antonia L, Davoren G (2008) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:289–303. doi:10.3354/meps07221

    Article  Google Scholar 

  • Elliott KH, Bull RD, Gaston AJ, Davoren GK (2009a) Underwater and above-water search patterns of an Arctic seabird: reduced searching at small spatiotemporal scales. Behav Ecol Sociobiol 63:1773–1785. doi:10.1007/s00265-009-0801-y

    Article  Google Scholar 

  • Elliott KH, Woo KJ, Gaston AJ (2009b) Specialization in murres: the story of eight specialists. Waterbirds 32:491–506. doi:10.1675/063.032.0402

    Article  Google Scholar 

  • Elliott KH, Le Vaillant M, Kato A, Gaston AJ, Ropert-Coudert Y, Hare JF, Speakman JR, Croll D (2014a) Age-related variation in energy expenditure in a long-lived bird within the envelope of an energy ceiling. J Anim Ecol 83:136–146. doi:10.1111/1365-2656.12126

    Article  Google Scholar 

  • Elliott KH, O’Reilly KM, Hatch SA, Gaston AJ, Hare JF, Anderson WG (2014b) The prudent parent meets old age: a high stress response in very old seabirds supports the terminal restraint hypothesis. Horm Behav 66:828–837. doi:10.1016/j.yhbeh.2014.11.001

    Article  CAS  Google Scholar 

  • Evans JC, Votier SC, Dall SRX (2015) Information use in colonial living. Biol Rev. doi:10.1111/brv.12188

    Google Scholar 

  • Fifield DA, Montevecchi WA, Garthe S, Robertson GJ, Kubetzki U, Rail JF (2014) Migratory tactics and wintering areas of northern gannets (Morus bassanus) breeding in North America. Ornithol Monogr 79:1–63

    Google Scholar 

  • Furness RW, Crane JE, Bearhop S, Garthe S, Käkelä A, Käkelä R, Kelly A, Kubetzki U, Votier SC, Waldron S (2006) Techniques to link individual migration patterns of seabirds with diet specialization, condition and breeding performance. Ardea 94:631–638

    Google Scholar 

  • Golet G, Kuletz K, Roby D, Irons D (2000) Adult prey choice affects chick growth and reproductive success in pigeon guillemots. Auk 117:82–91

    Article  Google Scholar 

  • Granadeiro JP, Phillips RA, Brickle P, Catry P (2011) Albatrosses following fishing vessels: how badly hooked are they on an easy meal? PLoS ONE 6:e17467. doi:10.1371/journal.pone.0017467

    Article  CAS  Google Scholar 

  • Granadeiro JP, Brickle P, Catry P (2014) Do individual seabirds specialize in fisheries’ waste? The case of black-browed albatrosses foraging over the Patagonian Shelf. Anim Conserv 17:19–26. doi:10.1111/acv.12050

    Article  Google Scholar 

  • Grémillet D, Wilson RP, Storch S, Gary Y (1999) Three-dimensional space utilization by a marine predator. Mar Ecol Prog Ser 183:263–273

    Article  Google Scholar 

  • Grist H, Daunt F, Wanless S, Nelson EJ, Harris MP, Newell M, Burthe S, Reid JM (2014) Site fidelity and individual variation in winter location in partially migratory European shags. PLoS ONE 9:e98562. doi:10.1371/journal.pone.0098562

    Article  CAS  Google Scholar 

  • Guilford T, Freeman R, Boyle D, Dean B, Kirk H, Phillips R, Perrins C (2011) A dispersive migration in the Atlantic puffin and its implications for migratory navigation. PLoS ONE 6:e21336. doi:10.1371/journal.pone.0021336

    Article  CAS  Google Scholar 

  • Hamer K, Phillips R, Hill J (2001) Contrasting foraging strategies of gannets Morus bassanus at two North Atlantic colonies: foraging trip duration and foraging area fidelity. Mar Ecol Prog Ser 224:283–290

    Article  Google Scholar 

  • Hamer K, Humphreys E, Garthe S, Hennicke J, Peters G, Grémillet D, Phillips R, Harris M, Wanless S (2007) Annual variation in diets, feeding locations and foraging behaviour of gannets in the North Sea: flexibility, consistency and constraint. Mar Ecol Prog Ser 338:295–305. doi:10.3354/meps338295

    Article  Google Scholar 

  • Harris S, Raya Rey A, Zavalaga C, Quintana F (2014) Strong temporal consistency in the individual foraging behaviour of imperial shags Phalacrocorax atriceps. Ibis 156:523–533. doi:10.1111/ibi.12159

    Article  Google Scholar 

  • Hedd A, Gales R, Brothers N (2001) Foraging strategies of shy albatross Thalassarche cauta breeding at Albatross Island, Tasmania, Australia. Mar Ecol Prog Ser 224:267–282

    Article  Google Scholar 

  • Helberg M, Systad G, Birkeland I, Lorentzen NH, Bustnes JO (2009) Migration patterns of adult and juvenile lesser black-backed gulls Larus fuscus from northern Norway. Ardea 97:281–286

    Article  Google Scholar 

  • Hobson KA, Clark RG (1993) Turnover of d13C in cellular and plasma reactions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641

    Article  Google Scholar 

  • Hunt GL, Wilson RP (2012) The coming of age of marine ornithology. Mar Ecol Prog Ser 451:227–229. doi:10.3354/meps09725

    Article  Google Scholar 

  • Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461. doi:10.1111/j.1474-919X.2008.00839.x

    Article  Google Scholar 

  • Irons D (1998) Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79:647–655

    Article  Google Scholar 

  • Jaeger A, Blanchard P, Richard P, Cherel Y (2009) Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar Biol 156:1233–1240. doi:10.1007/s00227-009-1165-6

    Article  Google Scholar 

  • Jaeger A, Connan M, Richard P, Cherel Y (2010) Use of stable isotopes to quantify seasonal changes of trophic niche and levels of population and individual specialisation in seabirds. Mar Ecol Prog Ser 401:269–277. doi:10.3354/meps08380

    Article  CAS  Google Scholar 

  • Jouventin P, Bried J (2001) The effect of mate choice on speciation in snow petrels. Anim Behav 62:123–132. doi:10.1006/anbe.2001.1713

    Article  Google Scholar 

  • Käkelä A, Crane J, Votier S, Furness RW, Käkelä R (2006) Fatty acid signatures as indicators of diet in great skuas Stercorarius skua, Shetland. Mar Ecol Prog Ser 319:297–310. doi:10.3354/meps319297

    Article  Google Scholar 

  • Käkelä A, Furness R, Kelly A, Strandberg U, Waldron S, Käkelä R (2007) Fatty acid signatures and stable isotopes as dietary indicators in North Sea seabirds. Mar Ecol Prog Ser 342:291–301. doi:10.3354/meps342291

    Article  Google Scholar 

  • Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P, Naito Y (2000) Variation in foraging and parental behavior of king cormorants. Auk 117:718–730

    Article  Google Scholar 

  • Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2006) A mechanistic link between chick diet and decline in seabirds? Proc R Soc B 273:445–450. doi:10.1098/rspb.2005.3351

    Article  CAS  Google Scholar 

  • Knoff AJ, Macko SA, Erwin RM (2001) Diets of nesting laughing gulls (Larus atricilla) at the Virginia Coast Reserve: observations from stable isotope analysis. Isot Environ Health Stud 37:67–88. doi:10.1080/10256010108033282

    Article  CAS  Google Scholar 

  • Kotzerka J, Hatch SA, Garthe S (2011) Evidence for foraging-site fidelity and individual foraging behavior of pelagic cormorants rearing chicks in the Gulf of Alaska. Condor 113:80–88. doi:10.1525/cond.2011.090158

    Article  Google Scholar 

  • Lecomte VJ, Sorci G, Cornet S, Jaeger A, Faivre B, Arnoux E, Gaillard M, Trouvé C, Besson D, Chastel O, Weimerskirch H (2010) Patterns of aging in the long-lived wandering albatross. Proc Natl Acad Sci USA 107:6370–6375. doi:10.1073/pnas.0911181107

    Article  CAS  Google Scholar 

  • Litzow M, Piatt JF, Abookire AA, Prichard AK, Robards MD (2000) Monitoring temporal and spatial variability in sandeel (Ammodytes hexapterus) abundance with pigeon guillemot (Cepphus columba) diets. ICES J Mar Sci 57:976–986. doi:10.1006/jmsc.2000.0583

    Article  Google Scholar 

  • Mackley E, Phillips R, Silk J, Wakefield ED, Afanasyev V, Fox JW, Furness RW (2010) Free as a bird? Activity patterns of albatrosses during the nonbreeding period. Mar Ecol Prog Ser 406:291–303. doi:10.3354/meps08532

    Article  Google Scholar 

  • Magnusdottir E, Leat EHK, Bourgeon S, Strom H, Petersen A, Phillips RA, Hanssen SA, Bustnes JO, Hersteinsson P, Furness RW (2012) Wintering areas of great skuas Stercorarius skua breeding in Scotland, Iceland and Norway. Bird Study 59:1–9. doi:10.1080/00063657.2011.636798

    Article  Google Scholar 

  • Masello JF, Wikelski M, Voigt CC, Quillfeldt P (2013) Distribution patterns predict individual specialization in the diet of dolphin gulls. PLoS ONE 8:e67714. doi:10.1371/journal.pone.0067714

    Article  CAS  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305. doi:10.1111/j.1365-2656.2010.01753.x

    Article  Google Scholar 

  • McKnight A, Irons D, Allyn A, Sullivan K, Suryan R (2011) Winter dispersal and activity patterns of post-breeding black-legged kittiwakes Rissa tridactyla from Prince William Sound, Alaska. Mar Ecol Prog Ser 442:241–253. doi:10.3354/meps09373

    Article  Google Scholar 

  • Mehlum F, Watanuki Y, Takahashi A (2001) Diving behaviour and foraging habitats of Brunnich’s guillemots (Uria lomvia) breeding in the High-Arctic. J Zool 255:413–423

    Article  Google Scholar 

  • Montevecchi W, Benvenuti S, Garthe S, Davoren G, Fifield D (2009) Flexible foraging tactics by a large opportunistic seabird preying on forage and large pelagic fishes. Mar Ecol Prog Ser 385:295–306. doi:10.3354/meps08006

    Article  Google Scholar 

  • Moreno R, Jover L, Munilla I, Velando A, Sanpera C (2009) A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Mar Biol 157:545–553. doi:10.1007/s00227-009-1340-9

    Article  Google Scholar 

  • Muller M, Massa B, Phillips RA, Dell’Omo G (2014) Individual consistency and sex differences in migration strategies of Scopolis shearwaters (Calonectris diomedea) despite systematic year differences. Curr Zool 60:631–641

    Google Scholar 

  • Navarro J, González-Solís J (2009) Environmental determinants of foraging strategies in Cory’s shearwaters Calonectris diomedea. Mar Ecol Prog Ser 378:259–267. doi:10.3354/meps07880

    Article  CAS  Google Scholar 

  • Navarro J, Votier SC, Aguzzi J, Chiesa JJ, Forero MG, Phillips RA (2013) Ecological segregation in space, time and trophic niche of sympatric planktivorous petrels. PLoS ONE 8:e62897. doi:10.1371/journal.pone.0062897

    Article  CAS  Google Scholar 

  • Nelson JB (1980) Seabirds: their biology and ecology. Hamlyn, London 224 pp

    Google Scholar 

  • Newsome SD, Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436. doi:10.1890/060150.01

    Article  Google Scholar 

  • Oppel S, Beard A, Fox D, Mackley E, Leat E, Henry L, Clingham E, Fowler N, Sim J, Sommerfeld J, Weber N, Weber S, Bolton M (2015) Foraging distribution of a tropical seabird supports Ashmole’s hypothesis of population regulation. Behav Ecol Sociobiol. doi:10.1007/s00265-015-1903-3

    Google Scholar 

  • Oro D, de León A, Minguez E, Furness RW (2005) Estimating predation on breeding European storm-petrels (Hydrobates pelagicus) by yellow-legged gulls (Larus michahellis). J Zool 265:421–429. doi:10.1017/S0952836905006515

    Article  Google Scholar 

  • Patrick SC, Weimerskirch H (2014a) Consistency pays: sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird. Biol Lett 10:20140630. doi:10.1098/rsbl.2014.0630

    Article  Google Scholar 

  • Patrick SC, Weimerskirch H (2014b) Personality, foraging and fitness consequences in a long lived seabird. PLoS ONE 9:e87269. doi:10.1371/journal.pone.0087269

    Article  CAS  Google Scholar 

  • Patrick SC, Bearhop S, Grémillet D, Lescroël A, Grecian WJ, Bodey TW, Hamer KC, Wakefield E, Le Nuz M, Votier SC (2014) Individual differences in searching behaviour and spatial foraging consistency in a central place marine predator. Oikos 123:33–40. doi:10.1111/j.1600-0706.2013.00406.x

    Article  Google Scholar 

  • Pettex E, Lorentsen SH, Grémillet D, Gimenez O, Barret RT, Pons J-B, Le Bohec C, Bonadonna F (2012) Multi-scale foraging variability in northern gannet (Morus bassanus) fuels potential foraging plasticity. Mar Biol 159:2743–2756. doi:10.1007/s00227-012-2035-1

    Google Scholar 

  • Phillips R, Silk J, Croxall J (2005) Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology 86:2386–2396

    Article  Google Scholar 

  • Phillips RA, Silk JRD, Croxall JP, Afanasyev V (2006) Year-round distribution of white-chinned petrels from South Georgia: relationships with oceanography and fisheries. Biol Conserv 129:336–347. doi:10.1016/j.biocon.2005.10.046

    Article  Google Scholar 

  • Phillips R, Catry P, Silk J, Bearhop S, McGill R, Afanasyev V, Strange I (2007) Movements, winter distribution and activity patterns of Falkland and brown skuas: insights from loggers and isotopes. Mar Ecol Prog Ser 345:281–291. doi:10.3354/meps06991

    Article  Google Scholar 

  • Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208. doi:10.1007/s00227-011-1725-4

    Article  Google Scholar 

  • Pianka R (2011) Evolutionary ecology, 7th edn. Addison Wesley, San Francisco, p 512

    Google Scholar 

  • Pierotti R, Annett C (1991) Diet choice in the herring gull: constraints imposed by reproductive and ecological factors. Ecology 72:319–328

    Article  Google Scholar 

  • Pinaud D, Weimerskirch H (2005) Scale-dependent habitat use in a long-ranging central place predator. J Anim Ecol 74:852–863. doi:10.1111/j.1365-2656.2005.00984.x

    Article  Google Scholar 

  • Provencher JF, Elliott KH, Gaston AJ, Braune BM (2013) Networks of prey specialization in an Arctic monomorphic seabird. J Avian Biol 44:551–560. doi:10.1111/j.1600-048X.2013.05717.x

    Article  Google Scholar 

  • Quillfeldt P, McGill R, Masello J, Weiss F, Strange I, Brickle P, Furness RW (2008) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137–148. doi:10.3354/meps07751

    Article  Google Scholar 

  • Quillfeldt P, Voigt CC, Masello JF (2010) Plasticity versus repeatability in seabird migratory behaviour. Behav Ecol Sociobiol 64:1157–1164. doi:10.1007/s00265-010-0931-2

    Article  Google Scholar 

  • Ramos R, Ramírez F, Carrasco JL, Jover L (2011) Insights into the spatiotemporal component of feeding ecology: an isotopic approach for conservation management sciences. Divers Distrib 17:338–349. doi:10.1111/j.1472-4642.2010.00736.x

    Article  Google Scholar 

  • Ratcliffe N, Takahashi A, O’Sullivan C, Adlard S, Trathan PN, Harris MP, Wanless S (2013) The roles of sex, mass and individual specialisation in partitioning foraging-depth niches of a pursuit-diving predator. PLoS ONE 8:e79107. doi:10.1371/journal.pone.0079107

    Article  CAS  Google Scholar 

  • Ronconi R, Steenweg R, Taylor P, Mallory M (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. doi:10.3354/meps10980

    Article  CAS  Google Scholar 

  • Ropert-Coudert Y, Kato A, Naito Y, Cannell B (2003) Individual diving strategies in the little penguin. Waterbirds 4:403–408

    Article  Google Scholar 

  • Sanz-Aguilar A, Martínez-Abraín A, Tavecchia G, Mínguez E, Oro D (2009) Evidence-based culling of a facultative predator: efficacy and efficiency components. Biol Conserv 142:424–431. doi:10.1016/j.biocon.2008.11.004

    Article  Google Scholar 

  • Seltmann MW, Öst M, Jaatinen K, Atkinson S, Mashburn K, Hollmén T (2012) Stress responsiveness, age and body condition interactively affect flight initiation distance in breeding female eiders. Anim Behav 84:889–896. doi:10.1016/j.anbehav.2012.07.012

    Article  Google Scholar 

  • Soanes LM, Atkinson PW, Gauvain RD, Green JA (2013) Individual consistency in the foraging behaviour of northern gannets: implications for interactions with offshore renewable energy developments. Mar Policy 38:507–514. doi:10.1016/j.marpol.2012.08.006

    Article  Google Scholar 

  • Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012

    Google Scholar 

  • Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc B 274:839–844. doi:10.1098/rspb.2006.0198

    Article  Google Scholar 

  • Svanbäck R, Persson L (2004) Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. J Anim Ecol 73:973–982. doi:10.1111/j.0021-8790.2004.00868.x

    Article  Google Scholar 

  • Thompson DR, Hamer KC, Furness RW (1991) Mercury accumulation in great skuas Catharacta skua of known age and sex, and its effects upon breeding and survival. J Appl Ecol 28:672–684

    Article  Google Scholar 

  • Thomson J, Heithaus M, Burkholder D, Vaudo J, Wirsing A, Dill L (2012) Site specialists, diet generalists? Isotopic variation, site fidelity, and foraging by loggerhead turtles in Shark Bay, Western Australia. Mar Ecol Prog Ser 453:213–226. doi:10.3354/meps09637

    Article  Google Scholar 

  • Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci USA 105:560–565. doi:10.1073/pnas.0709263105

    Article  CAS  Google Scholar 

  • Tranquilla LA, Montevecchi WA, Fifield DA, Hedd A, Gaston AJ, Robertson GJ, Phillips RA (2014) Individual winter movement strategies in two species of murre (Uria spp.) in the Northwest Atlantic. PLoS ONE 9:e90583. doi:10.1371/journal.pone.0090583

    Article  CAS  Google Scholar 

  • Van de Pol M, Brouwer L, Ens BJ, Oosterbeek K, Tinbergen JM (2010) Fluctuating selection and the maintenance of individual and sex-specific diet specialization in free-living oystercatchers. Evolution 64:836–851. doi:10.1111/j.1558-5646.2009.00859.x

    Article  Google Scholar 

  • Van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc B 271:65–73. doi:10.1098/rspb.2003.2518

    Article  Google Scholar 

  • Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714. doi:10.1098/rsbl.2010.0124

    Article  Google Scholar 

  • Votier SC, Bearhop S, Ratcliffe N, Phillips RA, Furness RW (2004a) Predation by great skuas at a large Shetland seabird colony. J Appl Ecol 41:1117–1128. doi:10.1111/j.0021-8901.2004.00974.x

    Article  Google Scholar 

  • Votier SC, Bearhop S, Ratcliffe N, Furness RW (2004b) Reproductive consequences for great skuas specializing as seabird predators. Condor 106:275–287

    Article  Google Scholar 

  • Votier SC, Bearhop S, Crane JE, Arcos M, Furness RW (2007) Seabird predation by great skuas Stercorarius skua - intra-specific competition for food? J Avian Biol 38:234–246. doi:10.1111/j.2007.0908-8857.03893.x

    Article  Google Scholar 

  • Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, Newton J (2010a) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497. doi:10.1111/j.1365-2664.2010.01790.x

    Article  Google Scholar 

  • Votier SC, Grecian WJ, Patrick S, Newton J (2010b) Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis. Mar Biol 158:355–362. doi:10.1007/s00227-010-1563-9

    Article  CAS  Google Scholar 

  • Wakefield E, Phillips R, Trathan P, Arata J, Gales R, Huin N, Roberson G, Waugh SM, Weimerskirch H, Matthiopoulos J (2011) Habitat preference, accessibility, and competition limit the global distribution of breeding black-browed albatrosses. Ecol Monogr 81:141–167

    Article  Google Scholar 

  • Wakefield ED, Bodey TW, Bearhop S, Blackburn J, Colhoun K, Davies R, Dwyer RG, Green JA, Grémillet D, Jackson AL, Jessopp MJ, Kane A, Langston RH, Lescroël A, Murray S, Le Nuz M, Patrick SC (2013) Space partitioning without territoriality in gannets. Science 341:68–70. doi:10.1126/science.1236077

    Article  CAS  Google Scholar 

  • Wakefield ED, Cleasby IR, Bearhop S, Bodey TW, Davies RD, Miller PI, Newton J, Votier SC, Hamer KC (in press) Long-term individual foraging site fidelity—why some gannets don’t change their spots. Ecology

  • Wanless S, Harris MP, Morris JA (1990) A comparison of feeding areas used by individual common murres (Uria aalge), razorbills (Alca torda) and an Atlantic puffin (Fratercula arctica) during the breeding season. Colon Waterbirds 13:16–24

    Article  Google Scholar 

  • Watanuki Y (1992) Individual diet difference, parental care and reproductive success in slaty-backed gulls. Condor 94:159–171

    Article  Google Scholar 

  • Watanuki Y, Takahashi A, Sato K (2003) Feeding area specialization of chick-rearing Adélie penguins Pygoscelis adeliae in a fast sea-ice area. Ibis 145:558–564. doi:10.1046/j.1474-919X.2003.00165.x

    Article  Google Scholar 

  • Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Sea Res Part II Top Stud Oceanogr 54:211–223. doi:10.1016/j.dsr2.2006.11.013

    Article  Google Scholar 

  • Weimerskirch H, Salamolard M, Sarrazin F, Jouventin P (1993) Foraging strategy of wandering albatrosses through the breeding season: a study using satellite telemetry. Auk 110:325–342

    Google Scholar 

  • Weimerskirch H, Cherel Y, Delord K, Jaeger A, Patrick SC, Riotte-Lambert L (2014) Lifetime foraging patterns of the wandering albatross: life on the move! J Exp Mar Bio Ecol 450:68–78. doi:10.1016/j.jembe.2013.10.021

    Article  Google Scholar 

  • Woo KJ, Elliott KH, Davidson M, Gaston AJ, Davoren GK (2008) Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J Anim Ecol 77:1082–1091. doi:10.1111/j.1365-2656.2008.01429.x

    Article  Google Scholar 

  • Yamamoto T, Takahashi A, Sato K, Oka N, Yamamoto M, Trathan PN (2014) Individual consistency in migratory behaviour of a pelagic seabird. Behaviour 151:683–701. doi:10.1163/1568539X-00003163

    Article  Google Scholar 

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Acknowledgments

This research was cosponsored by the Foundation for Science and Technology (Portugal) and the European Social Fund (POPH, EU) through a postdoc grant to Filipe R. Ceia (SFRH/BPD/95372/2013). We are grateful to Stefan Garthe, Vitor Paiva, João C. Marques and José Xavier for discussion and insight on early draft of this manuscript which greatly improved this review. Comments and suggestions by Kyle Elliott, Thomas Bodey and one anonymous reviewer improved the manuscript.

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  1. MARE – Marine and Environmental Sciences Centre, Department of Life Sciences, University of Coimbra, 3004-517, Coimbra, Portugal

    Filipe R. Ceia & Jaime A. Ramos

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  1. Filipe R. Ceia
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Correspondence to Filipe R. Ceia.

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Responsible Editor: Y. Cherel.

Reviewed by K. H. Elliott, T. Bodey and an undisclosed expert.

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Ceia, F.R., Ramos, J.A. Individual specialization in the foraging and feeding strategies of seabirds: a review. Mar Biol 162, 1923–1938 (2015). https://doi.org/10.1007/s00227-015-2735-4

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