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Marine Biology

, Volume 162, Issue 10, pp 1923–1938 | Cite as

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

  • Filipe R. Ceia
  • Jaime A. Ramos
Review, concept, and synthesis

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.

Keywords

Stable Isotope Analysis Individual Specialization Ecological Implication Isotopic Niche Seabird Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human rights and animal standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 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 CrossRefGoogle Scholar
  2. Annett C, Pierotti R (1999) Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 87–88:19–25CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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
  12. 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 CrossRefGoogle Scholar
  13. Bolnick DI (2004) Can intraspecific competition drive disruptive selection? an experimental test in natural populations of sticklebacks. Evolution 58:608–618CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 60:497–514CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. Evans JC, Votier SC, Dall SRX (2015) Information use in colonial living. Biol Rev. doi: 10.1111/brv.12188 Google Scholar
  40. 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 79:1–63Google Scholar
  41. 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 94:631–638Google Scholar
  42. Golet G, Kuletz K, Roby D, Irons D (2000) Adult prey choice affects chick growth and reproductive success in pigeon guillemots. Auk 117:82–91CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Grémillet D, Wilson RP, Storch S, Gary Y (1999) Three-dimensional space utilization by a marine predator. Mar Ecol Prog Ser 183:263–273CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 224:283–290CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. Hedd A, Gales R, Brothers N (2001) Foraging strategies of shy albatross Thalassarche cauta breeding at Albatross Island, Tasmania, Australia. Mar Ecol Prog Ser 224:267–282CrossRefGoogle Scholar
  52. 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 97:281–286CrossRefGoogle Scholar
  53. Hobson KA, Clark RG (1993) Turnover of d13C in cellular and plasma reactions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641CrossRefGoogle Scholar
  54. Hunt GL, Wilson RP (2012) The coming of age of marine ornithology. Mar Ecol Prog Ser 451:227–229. doi: 10.3354/meps09725 CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. Irons D (1998) Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79:647–655CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P, Naito Y (2000) Variation in foraging and parental behavior of king cormorants. Auk 117:718–730CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 255:413–423CrossRefGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. 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 60:631–641Google Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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 CrossRefGoogle Scholar
  79. Nelson JB (1980) Seabirds: their biology and ecology. Hamlyn, London 224 pp Google Scholar
  80. 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 CrossRefGoogle Scholar
  81. 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
  82. 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 CrossRefGoogle Scholar
  83. 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 CrossRefGoogle Scholar
  84. 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 CrossRefGoogle Scholar
  85. 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 CrossRefGoogle Scholar
  86. 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
  87. Phillips R, Silk J, Croxall J (2005) Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology 86:2386–2396CrossRefGoogle Scholar
  88. 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 CrossRefGoogle Scholar
  89. 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 CrossRefGoogle Scholar
  90. 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 CrossRefGoogle Scholar
  91. Pianka R (2011) Evolutionary ecology, 7th edn. Addison Wesley, San Francisco, p 512Google Scholar
  92. Pierotti R, Annett C (1991) Diet choice in the herring gull: constraints imposed by reproductive and ecological factors. Ecology 72:319–328CrossRefGoogle Scholar
  93. 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 CrossRefGoogle Scholar
  94. 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 CrossRefGoogle Scholar
  95. 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 CrossRefGoogle Scholar
  96. 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 CrossRefGoogle Scholar
  97. 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 CrossRefGoogle Scholar
  98. 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 CrossRefGoogle Scholar
  99. 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 CrossRefGoogle Scholar
  100. Ropert-Coudert Y, Kato A, Naito Y, Cannell B (2003) Individual diving strategies in the little penguin. Waterbirds 4:403–408CrossRefGoogle Scholar
  101. 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 CrossRefGoogle Scholar
  102. 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 CrossRefGoogle Scholar
  103. 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 CrossRefGoogle Scholar
  104. Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012Google Scholar
  105. 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 CrossRefGoogle Scholar
  106. 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 CrossRefGoogle Scholar
  107. 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 28:672–684CrossRefGoogle Scholar
  108. 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 CrossRefGoogle Scholar
  109. 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 CrossRefGoogle Scholar
  110. 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 CrossRefGoogle Scholar
  111. 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 CrossRefGoogle Scholar
  112. 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 CrossRefGoogle Scholar
  113. 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 CrossRefGoogle Scholar
  114. 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 CrossRefGoogle Scholar
  115. Votier SC, Bearhop S, Ratcliffe N, Furness RW (2004b) Reproductive consequences for great skuas specializing as seabird predators. Condor 106:275–287CrossRefGoogle Scholar
  116. 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 CrossRefGoogle Scholar
  117. 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 CrossRefGoogle Scholar
  118. 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 CrossRefGoogle Scholar
  119. 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 81:141–167CrossRefGoogle Scholar
  120. 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 CrossRefGoogle Scholar
  121. 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. EcologyGoogle Scholar
  122. 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 13:16–24CrossRefGoogle Scholar
  123. Watanuki Y (1992) Individual diet difference, parental care and reproductive success in slaty-backed gulls. Condor 94:159–171CrossRefGoogle Scholar
  124. 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 CrossRefGoogle Scholar
  125. 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 CrossRefGoogle Scholar
  126. Weimerskirch H, Salamolard M, Sarrazin F, Jouventin P (1993) Foraging strategy of wandering albatrosses through the breeding season: a study using satellite telemetry. Auk 110:325–342Google Scholar
  127. 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 CrossRefGoogle Scholar
  128. 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 CrossRefGoogle Scholar
  129. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.MARE – Marine and Environmental Sciences Centre, Department of Life SciencesUniversity of CoimbraCoimbraPortugal

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