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Marine Biology

, 165:122 | Cite as

Constrained by consistency? Repeatability of foraging behavior at multiple timescales for a generalist marine predator

  • Elizabeth A. McHuron
  • Elliott Hazen
  • Daniel P. Costa
Original paper

Abstract

Marine predators frequently exhibit consistency in foraging behaviors despite the dynamic nature of marine ecosystems, which has the potential for ecological and evolutionary implications depending on the timescale at which it persists. We examined behavioral consistency in movements and diving behavior of adult female California sea lions (Zalophus californianus), which are abundant, generalist central-place foragers inhabiting an ecosystem characterized by small- and broad-scale oceanographic variability. We used biologging devices to measure repeatability of behavior within a season and stable isotope analysis of whiskers to quantify behavior across a 2-year period associated with anomalous environmental conditions that affected prey availability. Sea lions were significantly repeatable in all variables across multiple timescales (Radj = 0.26–0.82), although repeatability estimates were generally higher for variables related to characteristics of individual dives (e.g., dive depth) than those that described dive bouts (e.g., bout duration) or spatial use (e.g., volume of 3D utilization distribution). These differences may result from the fact that diving behaviors vary with prey type, whereas spatial use and bout variables may reflect the foraging success within prey patches or movement among patches. There was variation in how predictable individual sea lions were in their diving behaviors, which was largely unrelated or negatively related to foraging site fidelity. The strength of behavioral consistency decreased with time yet persisted across the 2-year period, suggesting that while sea lions alter their behavior in response to environmental change, the behavioral flexibility of individuals may ultimately be constrained by consistency.

Notes

Acknowledgements

We would like to acknowledge the US Navy and John Ugoretz for logistical support, S. Simmons, C. Kuhn, P. Robinson, M. Fowler, S. Peterson, L. Hückstädt, and the numerous field volunteers that helped with data collection. We also thank the reviewers whose comments improved the manuscript. Much of the data collection for this project was part of the Tagging of Pelagic Predators (TOPP) project, which was funded by Grants from the California Sea Grant Program, National Oceanographic Partnership Program, the Office of Naval Research, and the Moore, Packard, and Sloan Foundations. A Grant from the E & P Sound and Marine Life Joint Industry Programme (#22 07-23) to DPC and the Earl and Ethel Myers Oceanographic and Marine Biology Trust to EAM funded the remainder of this effort.

Funding

This study was funded by the E & P Sound and Marine Life Joint Industry Programme, the California Sea Grant Program, National Oceanographic Partnership Program, the Office of Naval Research, and the Moore, Packard, and Sloan Foundations.

Compliance with ethical standards

Ethical approval

Animal handling was permitted under appropriate permits (NMFS #87-1593, 1851, 17952) and approved by the University of California Santa Cruz Institutional Animal Care and Use Committee. All applicable, international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

227_2018_3382_MOESM1_ESM.pdf (660 kb)
Supplementary material 1 (PDF 660 kb)
227_2018_3382_MOESM2_ESM.pdf (116 kb)
Supplementary material 2 (PDF 115 kb)
227_2018_3382_MOESM3_ESM.pdf (162 kb)
Supplementary material 3 (PDF 162 kb)

References

  1. Abrahms B, Hazen EL, Bograd SJ, Brashares JS, Robinson PW, Scales KL, Crocker DE, Costa DP (2018) Climate mediates the success of migration strategies in a marine predator. Ecol Lett 21:63–71.  https://doi.org/10.1111/ele.12871 PubMedCrossRefGoogle Scholar
  2. Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958.  https://doi.org/10.1111/j.1461-0248.2011.01662.x PubMedCrossRefGoogle Scholar
  3. Arnould J, Boyd IL, Speakman JR (1996) The relationship between foraging behavior and energy expenditure in Antarctic fur seals. J Zool Soc Lond 239:769–782CrossRefGoogle Scholar
  4. Arnould J, Cherel Y, Gibbens J, White J, Littnan C (2011) Stable isotopes reveal inter-annual and inter-individual variation in the diet of female Australian fur seals. Mar Ecol Prog Ser 422:291–302.  https://doi.org/10.3354/meps08933 CrossRefGoogle Scholar
  5. Arthur B, Hindell M, Bester MN, Oosthuizen WC, Wege M, Lea MA (2016) South for the winter? Within-dive foraging effort reveals the trade-offs between divergent foraging strategies in a free-ranging predator. Funct Ecol 30:1623–1637.  https://doi.org/10.1111/1365-2435.12636 CrossRefGoogle Scholar
  6. Ballance LT, Ainley DG, Ballard G, Barton K (2009) An energetic correlate between colony size and foraging effort in seabirds, an example of the Adelie penguin Pygoscelis adeliae. J Avian Biol 40:279–288.  https://doi.org/10.1111/j.1600-048X.2008.04538.x CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.vo67.i01 CrossRefGoogle Scholar
  8. Baylis A, Page B, Goldsworthy S (2008) Colony-specific foraging areas of lactating New Zealand fur seals. Mar Ecol Prog Ser 361:279–290.  https://doi.org/10.3354/meps07258 CrossRefGoogle Scholar
  9. Baylis AMM, Orben RA, Arnould JPY, Peters K, Knox T, Costa DP, Staniland IJ (2015a) Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia 179:1053–1065.  https://doi.org/10.10007/s00442-015-3421-4 PubMedCrossRefGoogle Scholar
  10. Baylis AMM, Orben RA, Pistorius P, Brickle P, Staniland I, Ratcliffe N (2015b) Winter foraging site fidelity of king penguins breeding at the Falkland Islands. Mar Biol 162:99–110.  https://doi.org/10.1007/s00227-014-2561-0 CrossRefGoogle Scholar
  11. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783.  https://doi.org/10.1016/j.anbehav.2008.12.022 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanbäck R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941.  https://doi.org/10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2 CrossRefGoogle Scholar
  13. 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.  https://doi.org/10.1086/343878 PubMedCrossRefGoogle Scholar
  14. Boyd IL (1996) Temporal scales of foraging in a marine predator. Ecology 77:426–434.  https://doi.org/10.2307/2265619 CrossRefGoogle Scholar
  15. Boyd IL, Arnould JPY, Barton T, Croxall JP (1994) Foraging behavior of Antarctic fur seals during periods of contrasting prey abundance. J Anim Ecol 63:703–713CrossRefGoogle Scholar
  16. Boyd IL, McCafferty DJ, Walker TR (1997) Variation in foraging effort by lactating Antarctic fur seals: response to simulated increased foraging costs. Behav Ecol Sociobiol 40:135–144.  https://doi.org/10.1007/s002650050326 CrossRefGoogle Scholar
  17. Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519CrossRefGoogle Scholar
  18. Camprasse ECM, Sutton GJ, Berlincourt M, Arnould JPY (2017) Changing with the times: little penguins exhibit flexibility in foraging behaviour and low behavioural consistency. Mar Biol 164:1–10.  https://doi.org/10.1007/s00227-017-3193-y CrossRefGoogle Scholar
  19. Carneiro APB, Bonnet-Lebrun A-S, Manica A, Staniland IJ, Phillips RA (2017) Methods for detecting and quantifying individual specialisation in movement and foraging strategies of marine predators. Mar Ecol Prog Ser 578:151–166CrossRefGoogle Scholar
  20. Ceia FR, Ramos JA (2015) Individual specialization in the foraging and feeding strategies of seabirds: a review. Mar Biol 162:1923–1938.  https://doi.org/10.1007/s00227-015-2735-4 CrossRefGoogle Scholar
  21. Charnov E (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136PubMedCrossRefGoogle Scholar
  22. Checkley DM, Barth JA (2009) Patterns and processes in the California Current System. Prog Oceanogr 83:49–64.  https://doi.org/10.1016/j.pocean.2009.07.028 CrossRefGoogle Scholar
  23. Cherel Y, Kernaléguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol Lett 5:830–832.  https://doi.org/10.1098/rsbl.2009.0552 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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.  https://doi.org/10.1007/s00300-005-0089-y CrossRefGoogle Scholar
  25. Cooper NW, Sherry TW, Marra PP (2014) Modeling three-dimensional space use and overlap in birds. Auk 131:681–693.  https://doi.org/10.1642/AUK-14-17.1 CrossRefGoogle Scholar
  26. Costa DP (2008) A conceptual model of the variation in parental attendance in response to environmental fluctuation: foraging energetics of lactating sea lions and fur seals. Aquat Conserv Mar Freshw Ecosyst 17:S44–S52.  https://doi.org/10.1002/aqc CrossRefGoogle Scholar
  27. Costa DP, Gales NJ (2000) Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. J Exp Biol 203:3655–3665PubMedGoogle Scholar
  28. Costa DP, Croxall JP, Duck CD (1989) Foraging energetics of Antarctic fur seals in relation to changes in prey availability. Ecology 70:596–606CrossRefGoogle Scholar
  29. Costa DP, Robinson PW, Arnould JPY, Harrison A-L, Simmons SE, Hassrick JL, Hoskins AJ, Kirkman SP, Oosthuizen H, Villegas-Amtmann S, Crocker DE (2010) Accuracy of ARGOS locations of pinnipeds at-sea estimated using Fastloc GPS. PLoS ONE 5:e8677.  https://doi.org/10.1371/journal.pone.0008677 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subarctic islands from grassland to tundra. Science (80-) 307:1959–1961.  https://doi.org/10.1126/science.1108485 CrossRefGoogle Scholar
  31. Croxall JP, Reid K, Prince PA (1999) Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar Ecol Prog Ser 177:115–131.  https://doi.org/10.3354/meps177115 CrossRefGoogle Scholar
  32. Dall SRX, Bell AM, Bolnick DI, Ratnieks FLW (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198.  https://doi.org/10.1111/j.1461-0248.2012.01846.x PubMedPubMedCentralCrossRefGoogle Scholar
  33. Davoren GK, Montevecchi WA (2003) Consequences of foraging trip duration on provisioning behaviour and fledging condition of common murres Uria aalgae. J Avian Biol 34:44–53.  https://doi.org/10.1034/j.1600-048X.2003.03008.x CrossRefGoogle Scholar
  34. Davoren GK, Montevecchi WA, Anderson JT (2003) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481.  https://doi.org/10.1890/02-0208 CrossRefGoogle Scholar
  35. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54.  https://doi.org/10.1111/1365-2656.12013 PubMedCrossRefGoogle Scholar
  36. Doniol-Valcroze T, Lesage V, Giard J, Michaud R (2011) Optimal foraging theory predicts diving and feeding strategies of the largest marine predator. Behav Ecol 22:880–888.  https://doi.org/10.1093/beheco/arr038 CrossRefGoogle Scholar
  37. Duong T (2018) ks: Kernel smoothing. R package version 1.11.0. https://CRAN.R-project.org/package=ks
  38. Elliott KH, Woo K, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK (2008) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:289–303.  https://doi.org/10.3354/meps07221 CrossRefGoogle Scholar
  39. Feldkamp SD, DeLong RL, Antonelis GA (1989) Diving patterns of California sea lions, Zalophus californianus. Can J Zool 67:872–883.  https://doi.org/10.1139/z89-129 CrossRefGoogle Scholar
  40. Fieberg J, Kochanny CO (2005) Quantifying home-range overlap: the importance of the utilization distribution. J Wildl Manag 69:1346–1359CrossRefGoogle Scholar
  41. Foo D, Semmens JM, Arnould JPY, Dorville N, Hoskins AJ, Abernathy K, Marshall GJ, Hindell MA (2016) Testing optimal foraging theory models on benthic divers. Anim Behav 112:127–138.  https://doi.org/10.1016/j.anbehav.2015.11.028 CrossRefGoogle Scholar
  42. Gales NJ, Mattlin RH (1998) Fast, safe, field-portable gas anesthesia for otariids. Mar Mamm Sci 14:355–361.  https://doi.org/10.1111/j.1748-7692.1998.tb00727.x CrossRefGoogle Scholar
  43. Garthe S, Montevecchi WA, Chapdelaine G, April JR (2007) Contrasting foraging tactics by northern gannets (Sula bassana) breeding in different oceanographic domains with different prey fields. Mar Biol 151:687–694.  https://doi.org/10.1007/s00227-006-0523-x CrossRefGoogle Scholar
  44. Grémillet D, Dell’Omo G, Ryan PG, Peters G, Ropert-Coudert Y, Weeks SJ (2004) Offshore diplomacy or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape Gannets from neighbouring breeding sites. Mar Ecol Prog Ser 268:265–279.  https://doi.org/10.3354/meps268265 CrossRefGoogle Scholar
  45. Hamer KC, Phillips RA, Hill JK, Wanless S, Wood AG (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.  https://doi.org/10.3354/meps224283 CrossRefGoogle Scholar
  46. Harris S, Raya Rey A, Zavalaga C, Quintana F (2014) Strong temporal consistency in the individual foraging behaviour of Imperial Shags Phalacrocorax atriceps. Ibis (Lond 1859) 156:523–533.  https://doi.org/10.1111/ibi.12159 CrossRefGoogle Scholar
  47. Hazen EL, Maxwell SM, Bailey H, Bograd SJ, Hamann M, Gaspar P, Godley BJ, Shillinger GL (2012) Ontogeny in marine tagging and tracking science: technologies and data gaps. Mar Ecol Prog Ser 457:221–240.  https://doi.org/10.3354/meps09857 CrossRefGoogle Scholar
  48. Heaslip SG, Bowen WD, Iverson SJ (2014) Testing predictions of optimal diving theory using animal-borne video from harbour seals (Phoca vitulina concolor). Can J Zool 92:309–318.  https://doi.org/10.1139/cjz-2013-0137 CrossRefGoogle Scholar
  49. Hoskins AJ, Costa DP, Wheatley KE, Gibbens JR, Arnould JPY (2015) Influence of intrinsic variation on foraging behaviour of adult female Australian fur seals. Mar Ecol Prog Ser 526:227–239.  https://doi.org/10.3354/meps11200 CrossRefGoogle Scholar
  50. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363PubMedCrossRefGoogle Scholar
  51. Hückstädt LA, Koch PL, McDonald BI, Goebel ME, Crocker DE, Costa DP (2012) Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169:395–406.  https://doi.org/10.1007/s00442-011-2202-y PubMedCrossRefGoogle Scholar
  52. Hughes BB, Eby R, Dyke V, Tinker MT, Marks CI, Johnson KS, Wasson K (2013) Recovery of a top predator mediates negative eutrophic effects on seagrass. Proc Natl Acad Sci 110:15313–15318.  https://doi.org/10.1073/pnas.1302805110 PubMedCrossRefGoogle Scholar
  53. Johnson D, London J, Lea M, Durban J (2008) Continuous-time correlated random walk model for animal telemetry data. Ecology 89:1208–1215PubMedCrossRefGoogle Scholar
  54. Katzner TE, Bragin EA, Knick ST, Smith AT (2005) Relationship between demographics and diet specificity of Imperial Eagles Aquila heliaca in Kazakhstan. Ibis (Lond 1859) 147:576–586.  https://doi.org/10.1111/j.1474-919x.2005.00443.x CrossRefGoogle Scholar
  55. Kernaleguen L, Arnould JP, Guinet C, Cazelles B, Richard P, Cherel Y (2016) Early-life sexual segregation: ontogeny of isotopic niche differentiation in the Antarctic fur seal. Sci Rep 6:33211.  https://doi.org/10.1038/srep33211 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kernaléguen L, Cazelles B, Arnould JPY, Richard P, Guinet C, Cherel Y (2012) Long-term species, sexual and individual variations in foraging strategies of fur seals revealed by stable isotopes in whiskers. PLoS ONE 7:e32916.  https://doi.org/10.1371/journal.pone.0032916 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kernaléguen L, Arnould JPY, Guinet C, Cherel Y (2015) Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals. J Anim Ecol 84:1081–1091PubMedCrossRefGoogle Scholar
  58. Kernaléguen L, Dorville N, Ierodiaconou D, Hoskins AJ, Baylis AMM, Hindell MA, Semmens J, Abernathy K, Marshall GJ, Cherel Y, Arnould JPY (2016) From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialisation in Australian fur seals. Oecologia 180:657–670.  https://doi.org/10.1007/s00442-015-3407-2 PubMedCrossRefGoogle Scholar
  59. Knudsen R, Primicerio R, Amundsen PA, Klemetsen A (2010) Temporal stability of individual feeding specialization may promote speciation. J Anim Ecol 79:161–168.  https://doi.org/10.1111/j.1365-2656.2009.01625.x PubMedCrossRefGoogle Scholar
  60. Kuhn CE, Ream RR, Sterling JT, Thomason JR, Towell RG (2014) Spatial segregation and the influence of habitat on the foraging behavior of northern fur seals (Callorhinus ursinus). Can J Zool 92:861–873.  https://doi.org/10.1139/cjz-2014-0087 CrossRefGoogle Scholar
  61. Laake JL, Lowry MS, Delong RL, Melin SR, Carretta JV (2018) Population growth and status of California sea lions in the US. J Wildl Manag.  https://doi.org/10.1002/jwmg.21405 CrossRefGoogle Scholar
  62. Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18CrossRefGoogle Scholar
  63. Lowry MS, Melin S, Laake J (2017) Breeding season distribution and population growth of California sea lions, Zalophus californianus, in the United States during 1964–2014. NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC 574Google Scholar
  64. Lowther A, Harcourt R, Hamer D, Goldsworthy S (2011) Creatures of habit: foraging habitat fidelity of adult female Australian sea lions. Mar Ecol Prog Ser 443:249–263.  https://doi.org/10.3354/meps09392 CrossRefGoogle Scholar
  65. Lowther AD, Harcourt RG, Page B, Goldsworthy SD (2013) Steady as he goes: at-sea movement of adult male Australian sea lions in a dynamic marine environment. PLoS ONE.  https://doi.org/10.1371/journal.pone.0074348 CrossRefPubMedPubMedCentralGoogle Scholar
  66. McClatchie S, Field J, Thompson AR, Gerrodette T, Lowry M, Fiedler PC, Nieto KM, Vetter RD (2016a) Food limitation of sea lion pups and the decline of forage off central and southern California. R Soc Open Sci 3:150628.  https://doi.org/10.1098/rsos.150628 PubMedPubMedCentralCrossRefGoogle Scholar
  67. McClatchie S, Goericke R, Leising AW, Auth TD, Bjorkstedt E, Robertson R, Brodeur RD, Du X, Daly EA, Morgan CA, Chavez FP, Debich A, Hilderbrand J, Field J, Sakuma K, Jacox MG, Kahru M, Kudela RM, Anderson C, Lavaniegos B, Gomez-Valdes J, Jimenez-Rosenberg SPA, McCabe R, Melin SR, Ohman MD, Sala LM, Peterson B, Fisher J, Schroeder ID, Bograd SJ, Hazen EL, Schneider SR, Golightly RT, Suryan RM, Gladics AJ, Loredo S, Porquez JM, Thompson AR, Weber ED, Watson W, Trainer V, Wwarzybok P, Bradley R, Jahncke J (2016b) State of the California Current 2015–16: comparisons with the 1997–98 El Niño. Calif Coop Ocean Fish Investig Rep 57:5–61Google Scholar
  68. McHuron EA, Robinson PW, Simmons SE, Kuhn CE, Fowler M, Costa DP (2016a) Foraging strategies of a generalist marine predator inhabiting a dynamic environment. Oecologia 182:995–1005.  https://doi.org/10.1007/s00442-016-3732-0 PubMedCrossRefGoogle Scholar
  69. McHuron EA, Walcott SM, Zeligs J, Skrovan S, Costa DP, Reichmuth C (2016b) Whisker growth dynamics in two North Pacific pinnipeds: implications for determining foraging ecology from stable isotope analysis. Mar Ecol Prog Ser 554:213–224.  https://doi.org/10.3354/meps11793 CrossRefGoogle Scholar
  70. McHuron E, Mangel M, Schwarz LK, Costa DP (2017) Energy and prey requirements of California sea lions under variable environmental conditions. Mar Ecol Prog Ser 567:235–247CrossRefGoogle Scholar
  71. McHuron EA, Peterson SH, Hückstädt LA, Melin SR, Harris JD, Costa DP (2018) The energetic consequences of behavioral variation in a marine carnivore. Ecol Evol.  https://doi.org/10.1002/ece3.3983 CrossRefPubMedPubMedCentralGoogle Scholar
  72. McIntyre T, Bester MN, Bornemann H, Tosh CA, de Bruyn PJN (2017) Slow to change? Individual fidelity to three-dimensional foraging habitats in southern elephant seals, Mirounga leonina. Anim Behav 127:91–99.  https://doi.org/10.1016/j.anbehav.2017.03.006 CrossRefGoogle Scholar
  73. Melin S, DeLong R, Siniff D (2008) The effects of El Niño on the foraging behavior of lactating California sea lions (Zalophus californianus californianus) during the nonbreeding season. Can J Zool 86:192–206.  https://doi.org/10.1139/Z07-132 CrossRefGoogle Scholar
  74. Mori Y, Boyd IL (2004) The behavioral basis for nonlinear functional responses and optimal foraging in Antarctic fur seals. Ecology 85:398–410CrossRefGoogle Scholar
  75. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc 85:935–956.  https://doi.org/10.1111/j.1469-185X.2010.00141.x PubMedCrossRefGoogle Scholar
  76. Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974PubMedCrossRefGoogle Scholar
  77. Newsome SD, Tinker MT, Gill VA, Hoyt ZN, Doroff A, Nichol L, Bodkin JL (2015) The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters. Oecologia 178:45–59.  https://doi.org/10.1007/s00442-015-3223-8 PubMedCrossRefGoogle Scholar
  78. Novak M, Tinker MT (2015) Timescales alter the inferred strength and temporal consistency of intraspecific diet specialization. Oecologia 178:61–74.  https://doi.org/10.1007/s00442-014-3213-2 PubMedCrossRefGoogle Scholar
  79. Orr A, VanBlaricom G, DeLong R, Cruz-Escalona V, Newsome S (2011) Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses. Can J Zool 89:109–122.  https://doi.org/10.1139/Z10-101 CrossRefGoogle Scholar
  80. Patrick SC, Weimerskirch H (2014a) Consistency pays: sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird. Biol Lett 10:20140630.  https://doi.org/10.1098/rsbl.2014.0630 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Patrick SC, Weimerskirch H (2014b) Personality, foraging and fitness consequences in a long lived seabird. PLoS ONE.  https://doi.org/10.1371/journal.pone.0087269 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Patrick SC, Weimerskirch H (2017) Reproductive success is driven by local site fidelity despite stronger specialisation by individuals for large-scale habitat preference. J Anim Ecol 86:674–682.  https://doi.org/10.1111/1365-2656.12636 PubMedCrossRefGoogle Scholar
  83. 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.  https://doi.org/10.1111/j.1600-0706.2013.00406.x CrossRefGoogle Scholar
  84. 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 46:1–10.  https://doi.org/10.1111/jav.00660 CrossRefGoogle Scholar
  85. Patrick SC, Pinaud D, Weimerskirch H (2017) Boldness predicts an individual’s position along an exploration–exploitation foraging trade-off. J Anim Ecol 86:1257–1268.  https://doi.org/10.1111/1365-2656.12724 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Potier S, Carpentier A, Grémillet D, Leroy B, Lescroël A (2015) Individual repeatability of foraging behaviour in a marine predator, the great cormorant, Phalacrocorax carbo. Anim Behav 103:83–90.  https://doi.org/10.1016/j.anbehav.2015.02.008 CrossRefGoogle Scholar
  87. 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 8:1–7.  https://doi.org/10.1371/journal.pone.0079107 CrossRefGoogle Scholar
  88. Rea LD, Christ A, Hayden A, Stegall V, Farley S, Stricker C, Mellish J-AE, Maniscalco JM, Waite J, Burkanov V (2015) Age-specific vibrissae growth rates: a tool for determining the timing of ecologically important events in Steller sea lions. Mar Mamm Sci 31:1213–1233.  https://doi.org/10.1111/mms.12221 CrossRefGoogle Scholar
  89. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318.  https://doi.org/10.1111/j.1469-185X.2007.00010.x PubMedCrossRefGoogle Scholar
  90. Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP et al (2014) Status and ecological effects of the world’s largest carnivores. Science (80-) 343:1241484.  https://doi.org/10.1126/science.1241484 CrossRefGoogle Scholar
  91. Roman J, Estes JA, Morissette L, Smith C, Costa D, McCarthy J, Nation JB, Nicol S, Pershing A, Smetacek V (2014) Whales as marine ecosystem engineers. Front Ecol Environ 12:377–385.  https://doi.org/10.1890/130220 CrossRefGoogle Scholar
  92. Rossman S, Ostrom PH, Stolen M, Barros NB, Gandhi H, Stricker CA, Wells RS (2015) Individual specialization in the foraging habits of female bottlenose dolphins living in a trophically diverse and habitat rich estuary. Oecologia 178:415–425.  https://doi.org/10.1007/s00442-015-3241-6 PubMedCrossRefGoogle Scholar
  93. Schakner ZA, Petelle MB, Tennis MJ, Van der Leeuw BK, Stansell RT, Blumstein DT (2017) Social associations between California sea lions influence the use of a novel foraging ground. R Soc Open Sci 4:160820.  https://doi.org/10.1098/rsos.160820 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Sigler MF, Gende SM, Csepp DJ (2017) Association of foraging Steller sea lions with persistent prey hot spots in southeast Alaska. Mar Ecol Prog Ser 571:233–243.  https://doi.org/10.3354/meps12145 CrossRefGoogle Scholar
  95. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378.  https://doi.org/10.1016/j.tree.2004.04.009 PubMedCrossRefGoogle Scholar
  96. Simpfendorfer CA, Olsen EM, Heupel MR, Moland E (2012) Three-dimensional kernel utilization distributions improve estimates of space use in aquatic animals. 572:565–572.  https://doi.org/10.1139/F2011-179 CrossRefGoogle Scholar
  97. Singmann H, Bolker B, Westfall J, Aust F (2018) afex: analysis of factorial experiments. R package version 0.19.1. https://CRAN.R-project.org/package=afex
  98. Staniland IJ, Reid K, Boyd IL (2004) Comparing individual and spatial influences on foraging behaviour in Antarctic fur seals Arctocephalus gazella. Mar Ecol Prog Ser 275:263–274.  https://doi.org/10.3354/meps275263 CrossRefGoogle Scholar
  99. Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol.  https://doi.org/10.1111/2041-210X.12797 CrossRefGoogle Scholar
  100. Suryan RM, Irons DB, Brown ED, Jodice PGR, Roby DD (2006) Site-specific effects on productivity of an upper trophic-level marine predator: bottom-up, top-down, and mismatch effects on reproduction in a colonial seabird. Prog Oceanogr 68:303–328.  https://doi.org/10.1016/j.pocean.2006.02.006 CrossRefGoogle Scholar
  101. Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc Biol Sci 274:839–844.  https://doi.org/10.1098/rspb.2006.0198 PubMedCrossRefGoogle Scholar
  102. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  103. Tinker MT, Costa DP, Estes JA, Wieringa N (2007) Individual dietary specialization and dive behaviour in the California sea otter: using archival time-depth data to detect alternative foraging strategies. Deep Res Part II Top Stud Oceanogr 54:330–342.  https://doi.org/10.1016/j.dsr2.2006.11.012 CrossRefGoogle Scholar
  104. 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.  https://doi.org/10.1073/pnas.0709263105 PubMedCrossRefGoogle Scholar
  105. 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 (NY) 64:836–851.  https://doi.org/10.1111/j.1558-5646.2009.00859.x CrossRefGoogle Scholar
  106. Villegas-Amtmann S, Costa D, Tremblay Y, Salazar S, Aurioles-Gamboa D (2008) Multiple foraging strategies in a marine apex predator, the Galapagos sea lion Zalophus wollebaeki. Mar Ecol Prog Ser 363:299–309.  https://doi.org/10.3354/meps07457 CrossRefGoogle Scholar
  107. Votier SC, Bearhop S, Ratcliff N, Furness RW (2004) Reproductive consequences for Great Skuas specializing as seabird predators.  https://doi.org/10.1650/7261 CrossRefGoogle Scholar
  108. Votier SC, Fayet AL, Bearhop S, Bodey TW, Clark BL, Grecian J, Guilford T, Hamer KC, Jeglinski JWE, Morgan G, Wakefield E, Patrick SC (2017) Effects of age and reproductive status on individual foraging site fidelity in a long-lived marine predator. Proc R Soc B Biol Sci 284:20171068.  https://doi.org/10.1098/rspb.2017.1068 CrossRefGoogle Scholar
  109. Wakefield ED, Cleasby IR, Bearhop S, Bodey TW, Davies RD, Miller PI, Newton J, Votier SC, Hamer KC (2015) Long-term individual foraging site fidelity—why some gannets don’t change their spot. Ecology 96:3058–3074.  https://doi.org/10.1890/14-1300.1 PubMedCrossRefGoogle Scholar
  110. Watanabe YY, Ito M, Takahashi A (2014) Testing optimal foraging theory in a penguin–krill system. Proc Biol Sci 281:20132376.  https://doi.org/10.1098/rspb.2013.2376 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Weise MJ, Costa DP, Kudela RM (2006) Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004. Geophys Res Lett 33:L22S10.  https://doi.org/10.1029/2006gl027113 CrossRefGoogle Scholar
  112. Whitfield DP, Reid R, Haworth PF, Madders M, Marquiss M, Tingay R, Fielding AH (2009) Diet specificity is not associated with increased reproductive performance of Golden Eagles Aquila chrysaetos in Western Scotland. Ibis (Lond 1859) 151:255–264.  https://doi.org/10.1111/j.1474-919x.2009.00924.x CrossRefGoogle Scholar
  113. Wilson AJ (2018) How should we interpret estimates of individual repeatability? Evol Lett 2:4–8.  https://doi.org/10.1002/evl3.40 CrossRefGoogle Scholar
  114. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461.  https://doi.org/10.1016/j.tree.2012.05.001 PubMedCrossRefGoogle Scholar
  115. 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.  https://doi.org/10.1111/j.1365-2656.2008.01429.x PubMedCrossRefGoogle Scholar
  116. Zhao L, Schell DM, Castellini MA (2006) Dietary macronutrients influence 13C and 15N signatures of pinnipeds: captive feeding studies with harbor seals (Phoca vitulina). Comp Biochem Physiol A Mol Integr Physiol 143:469–478.  https://doi.org/10.1016/j.cbpa.2005.12.032 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California Santa CruzSanta CruzUSA
  2. 2.Environmental Research DivisionNOAA Southwest Fisheries Science CenterMontereyUSA

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