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Marine Biology

, 166:83 | Cite as

High individual flexibility in the foraging behavior of a marine predator, the common murre

  • Julia GulkaEmail author
  • Gail K. Davoren
Original paper

Abstract

The foraging ecology of breeding seabirds is largely influenced by prey availability and energy demands related to reproduction which, in combination with other factors, can affect resource specialization in space and time. In this study, we combined GPS tracking, dive behavior, and stable isotope ratios of carbon and nitrogen to examine behavioral and dietary flexibility within individuals in a breeding pursuit-diving seabird, the common murre (Uria aalge), on the northeast Newfoundland coast. We examined individual flexibility over 2 years (2016, 2017) during which the timing of arrival and availability of their primary prey, capelin (Mallotus villosus), varied. In both years, we found high within-individual variation in foraging trip and dive characteristics, coupled with low spatial overlap of foraging trips both within and among individuals, indicative of flexible behavior. Concurrently, the isotopic niche of breeding common murres showed a higher degree of dietary consistency, evidenced by similar amounts of variation within and among individuals in stable isotope ratios (δ13C, δ15N). Dietary reconstruction revealed that the proportion of different prey types in the diet varied across individuals, suggesting a degree of dietary flexibility. When capelin (prey) availability was low (in 2017), foraging trips were longer and farther from the colony, maximum dive duration decreased, and the proportion of capelin in the diet decreased. Behavioral flexibility, however, remained similar across both years, regardless of prey availability. Our results suggest that common murres can tolerate and respond to fluctuations in prey availability through flexible foraging strategies. Increased foraging distances during low capelin availability suggest increased energetic costs, and thus, an energetic threshold may be reached above which lower prey availability cannot be tolerated.

Notes

Acknowledgements

Principal funding was provided by Natural Sciences and Engineering Research Council of Canada Discovery (2014-06290) and Ship Time Grants (486208-2016 and 501154-2017 to GKD), along with University of Manitoba Faculty of Science Fieldwork Support Program grants (2016, 2017) to GKD. Additional funding was provided by National Geographic Young Explorers Grant (WW-075ER-17) to JG and by World Wildlife Fund-Canada (G-0618-583-00-D) to GKD. GPS tags were partially funded by Environment and Climate Change Canada. We are indebted to the captain and crew of the Lady Easton for their assistance with fieldwork. Thanks to R. Ronconi for assistance with fieldwork, equipment, data analysis and comments on the manuscript; E. Jenkins, P. Calabria Carvalho, K. Johnson, L. Maynard, and W. Ogloff for assistance with field work; and J. Roth and the rest of the University of Manitoba Stable Isotopes in Ecology Group for guidance and feedback during data analysis. We would also like to thank the reviewers.

Data availability statement

The data sets analyzed during the current study are available from the corresponding author upon reasonable request.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which studies were conducted.

References

  1. Ainley DG, Nettleship DN, Carter HR, Storey AE (2002) Common Murre (Uria aalge). In: Rodewald PG (ed) The birds of North America Online. Cornell Lab of Ornithology, New YorkGoogle Scholar
  2. Anderson ORJ, Phillips RA, Shore RF, McGill RAR, McDonald RA, Bearhop S (2009) Diet, individual specialisation and breeding of brown skuas (Catharacta antarctica lonnbergi): an investigation using stable isotopes. Polar Biol 32:27–33Google Scholar
  3. Anderson HB, Evans PGH, Potts JM, Harris MP, Wanless S (2014) The diet of common guillemot Uria aalge chicks provides evidence of changing prey communities in the North Sea. Ibis (Lond 1859) 156:23–34Google Scholar
  4. Bairos-Novak KR, Crook KA, Davoren GK (2015) Relative importance of local enhancement as a search strategy for breeding seabirds: an experimental approach. Anim Behav 106:71–78Google Scholar
  5. Barquete V, Strauss V, Ryan PG (2013) Stable isotope turnover in blood and claws: a case study in captive African penguins. J Exp Mar Biol Ecol 448:121–127Google Scholar
  6. Bates D, Machler M, Bolker B, Walkter S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
  7. Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of lipid and uric acid on δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507Google Scholar
  8. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458PubMedGoogle Scholar
  9. Becker BH, Newman SH, Inglis S, Beissinger SR (2007) Diet–feather stable isotope (Δ15N and Δ13C) fractionation in common murres and other seabirds. Condor 109:451Google Scholar
  10. Bertrand S, Joo R, Arbulu Smet C, Tremblay Y, Barbraud C, Weimerskirch H (2012) Local depletion by a fishery can affect seabird foraging. J Appl Ecol 49:1168–1177Google Scholar
  11. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28PubMedGoogle Scholar
  12. Buckley NJ (1997) Spatial-concentration effects and the importance of local enhancement in the evolution of colonial breeding in seabirds. Am Nat 149:1091–1112PubMedGoogle Scholar
  13. Buren AD, Koen-Alonso M, Montevecchi WA (2012) Linking predator diet and prey availability: common murres and capelin in the Northwest Atlantic. Mar Ecol Prog Ser 445:25–35Google Scholar
  14. Buren AD, Koen-Alonso M, Pepin P, Mowbray F, Nakashima B, Stenson G, Ollerhead N, Montevecchi WA (2014) Bottom-up regulation of capelin, a keystone forage species. PLoS One 9:e87589PubMedPubMedCentralGoogle Scholar
  15. Burger AE (1997) Arrival and departure behavior of common murres at colonies: evidence for an information halo? Colon Waterbirds 20:55–65Google Scholar
  16. Burger AE, Piatt JF (1990) Flexible time budgets in breeding common murres: buffers against variable prey abundance. Stud Avian Biol 14:71–83Google Scholar
  17. Burke C (2008) Comparative foraging ecology of parental common murres (Uria aalge) and Atlantic puffins (Fratercula Arctica) in response to the changes in forage fish availability. Memorial University of NewfoundlandGoogle Scholar
  18. Burke CM, Montevecchi WA (2009) The foraging decisions of a central place foraging seabird in response to fluctuations in local prey conditions. J Zool 278:354–361Google Scholar
  19. Cairns DK (1988) Seabirds as indicators of marine food supplies. Biol Oceanogr 5:261–271Google Scholar
  20. Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519Google Scholar
  21. Camprasse ECM, Cherel Y, Arnould JPY, Hoskins AJ, Bost CA (2017) Combined bio-logging and stable isotopes reveal individual specialisations in a benthic coastal seabird, the Kerguelen shag. PLoS One 12:e0172278PubMedPubMedCentralGoogle Scholar
  22. Carneiro A, Bonnet-Lebrun A, Manica A, Staniland I, Phillips RA (2017) Methods for detecting and quantifying individual specialisation in movement and foraging strategies of marine predators. Mar Ecol Prog Ser 578:151–166Google Scholar
  23. Carscadden JE, Montevecchi WA, Davoren GK, Nakashima BS (2002) Trophic relationships among capelin (Mallotus villosus) and seabirds in a changing ecosystem. ICES J Mar Sci 59:1027–1033Google Scholar
  24. Cherel Y, Jaquemet S, Maglio A, Jaeger A (2014) Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237Google Scholar
  25. Crook KA, Maxner E, Davoren GK (2017) Temperature-based spawning habitat selection by capelin (Mallotus villosus) in Newfoundland. ICES J Mar Sci 74:1622–1629Google Scholar
  26. Cunningham J, Elliott K, Cottenie K, Hatch S, Jacobs S (2018) Individual foraging location, but not dietary, specialization: implications for rhinoceros auklets as samplers of forage fish. Mar Ecol Prog Ser 605:225–240Google Scholar
  27. Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85:265–271Google Scholar
  28. Davoren GK (2007) Effects of gill-net fishing on marine birds in a biological hotspot in the northwest Atlantic. Conserv Biol 21:1032–1045PubMedGoogle Scholar
  29. Davoren GK (2013a) Distribution of marine predator hotspots explained by persistent areas of prey. Mar Biol 160:3043–3058Google Scholar
  30. Davoren GK (2013b) Divergent use of spawning habitat by male capelin (Mallotus villosus) in a warm and cold year. Behav Ecol 24:152–161Google Scholar
  31. Davoren GK, Montevecchi WA (2003a) Consequences of foraging trip duration on provisioning behaviour and fledging condition of common murres Uria aalge. J Avian Biol 34:44–53Google Scholar
  32. Davoren GK, Montevecchi WA (2003b) Signals from seabirds indicate changing biology of capelin stocks. Mar Ecol Prog Ser 258:253–261Google Scholar
  33. Davoren GK, Montevecchi WA, Anderson JT (2003) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481Google Scholar
  34. Davoren GK, Anderson JT, Montevecchi WA (2006) Shoal behaviour and maturity relations of spawning capelin (Mallotus villosus) off Newfoundland: demersal spawning and diel vertical movement patterns. Can J Aquat Sci 63:268–284Google Scholar
  35. Davoren GK, Penton P, Burke C, Montevecchi WA (2012) Water temperature and timing of capelin spawning determine seabird diets. ICES J Mar Sci 69:1234–1241Google Scholar
  36. Dias MP, Granadeiro JP, Catry P (2013) Individual variability in the migratory path and stopovers of a long-distance pelagic migrant. Anim Behav 86:359–364Google Scholar
  37. Elliott KH, Ricklefs RE, Gaston AJ, Hatch SA, Speakman JR, Davoren GK (2013) High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins. Proc Natl Acad Sci USA 110:9380–9384PubMedGoogle Scholar
  38. Elliott KH, Roth JD, Crook K (2017) Lipid extraction techniques for stable isotope analysis and ecological assays. In: Bhattacharya SK (ed) Lipidomics: methods in molecular biology. Humana Press, New YorkGoogle Scholar
  39. Evans TJ, Kadin M, Olsson O, Åkesson S (2013) Foraging behaviour of common murres in the Baltic Sea, recorded by simultaneous attachment of GPS and time-depth recorder devices. Mar Ecol Prog Ser 475:277–289Google Scholar
  40. Fieberg J, Kochanny CO (2005) Quanitfying home-range overlap: the importance of the utilization distribution. J Wildl Manag 69:1346Google Scholar
  41. Garthe S, Montevecchi WA, Davoren GK (2011) Inter-annual changes in prey fields trigger different foraging tactics in a large marine predator. Limnol Oceanogr 56:802–812Google Scholar
  42. Grünbaum D, Veit RR (2003) Black-browed albatrosses foraging on Antarctic krill: density-dependence through local enhancement? Ecology 84:3265–3275Google Scholar
  43. Gulka J, Carvalho PC, Jenkins E, Johnson K, Maynard L, Davoren GK (2017) Dietary niche shifts of multiple marine predators under varying prey availability on the northeast Newfoundland coast. Front Mar Sci 4:324Google Scholar
  44. Hamer KC, Humphreys EM, Garthe S, Hennicke J, Peters G, Grémillet D, Phillips RA, Harris MP, 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 338:295–305Google Scholar
  45. Harding AMA, Piatt JF, Schmutz JA, Shultz MT, Van Pelt TI, Pelt V, Kettle AB, Speckman SG (2007a) Prey density and the behavioural flexibility of a marine predator: the common murre (Uria aalgae). Ecology 88:2024–2033PubMedGoogle Scholar
  46. Harding AMA, Piatt JF, Schmutz JA (2007b) Seabird behavior as an indicator of food supplies: sensitivity across the breeding season. Mar Ecol Prog Ser 352:269–274Google Scholar
  47. Harding A, Paredes R, Suryan R, Roby D, Irons D, Orben R, Renner H, Young R, Barger C, Dorresteijn I, Kitaysky A (2013) Does location really matter? An inter-colony comparison of seabirds breeding at varying distances from productive oceanographic features in the Bering Sea. Deep Res Part II Top Stud Oceanogr 94:178–191Google Scholar
  48. Harris MP, Wanless S (2011) The puffin. T & AD Poyser, LondonGoogle Scholar
  49. 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) 156:523–533Google Scholar
  50. Hedd A, Gales R, Brothers N (2001) Foraging strategies of shy albatross Thalassarche cauta breeding at Albatross Island, Tasmania, Australia. Mar Ecol Prog Ser 224:267–282Google Scholar
  51. Hedd A, Regular PM, Montevecchi WA, Buren AD, Burke CM, Fifield DA (2009) Going deep: common murres dive into frigid water for aggregated, persistent and slow-moving capelin. Mar Biol 156:741–751Google Scholar
  52. 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 169:395–406PubMedGoogle Scholar
  53. Irons DB (1998) Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79:647–655Google Scholar
  54. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602PubMedGoogle Scholar
  55. Kitaysky AS, Hunt J, Flint EN, Rubega MA, Decker MB (2000) Resource allocation in breeding seabirds: responses to fluctuations in their food supply. Mar Ecol Prog Ser 206:283–296Google Scholar
  56. Kokubun N, Takahashi A, Mori Y, Watanabe S, Shin HC (2010) Comparison of diving behavior and foraging habitat use between chinstrap and gentoo penguins breeding in the South Shetland Islands, Antarctica. Mar Biol 157:811–825Google Scholar
  57. Kokubun N, Takahashi A, Paredes R, Young RC, Sato NN, Yamamoto T, Kikuchi DM, Kitaiskaia EV, Ito M, Watanuki Y, Will AP, Lauth R, Romano MD, Kitaysky AS (2018) Inter-annual climate variability affects foraging behavior and nutritional state of thick-billed murres breeding in the southeastern Bering Sea. Mar Ecol Prog Ser 593:195–208Google Scholar
  58. Lavoie RA, Rail JF, Lean DRS (2012) Diet composition of seabirds from Corossol Island, Canada, using direct dietary and stable isotope analyses. Waterbirds 35:402–419Google Scholar
  59. Layman CA, Boucek R, Hammerschlag-peyer CM (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:542–562Google Scholar
  60. Linnebjerg JF, Fort J, Guilford T, Reuleaux A, Mosbech A, Frederiksen M (2013) Sympatric breeding auks shift between dietary and spatial resource partitioning across the annual cycle. PLoS One 8:e72987PubMedPubMedCentralGoogle Scholar
  61. Litzow MA, Piatt JF (2003) Variance in prey abundance influences time budgets of breeding seabirds: evidence from pigeon guillemots Cepphus columba. J Avian Biol 34(1):54–64Google Scholar
  62. Luque S, Guinet C (2007) A maximum likelihood approach for identifying dive bouts improves accuracy, precision and objectivity. Behaviour 144:1315–1332Google Scholar
  63. Macleod CJ, Adams J, Lyver P (2008) At-sea distribution of satellite-tracked grey-faced petrels, Pterodroma macroptera gouldi, captured on the Ruamaahua (Aldermen) Islands, New Zealand. Pap Proc R Soc Tasman 142:73Google Scholar
  64. Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305PubMedGoogle Scholar
  65. Monaghan P, Walton P, Wanless S, Uttley JD, Burns MD (1994) Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding guillemots Uria aalge. Ibis (Lond 1859) 136:214–222Google Scholar
  66. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480PubMedGoogle Scholar
  67. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  68. Patrick SC, Bearhop S, Gremillet D, Lescroel 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 123:33–40Google Scholar
  69. 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 46:431–440Google Scholar
  70. Penton PM, Davoren GK (2012) Physical characteristics of persistent deep- water spawning sites of capelin: importance for delimiting critical marine habitats. Mar Biol Res 8:778–783Google Scholar
  71. Pettex E, Lorentsen SH, Grémillet D, Gimenez O, Barrett RT, Pons JB, Le Bohec C, Bonadonna F (2012) Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity. Mar Biol 159:2743–2756Google Scholar
  72. Phillips R, Lewis S, Gonzalez-Solis J, Daunt F (2017) Causes and consequences of individual variability and specialization in foraging and migration strategies of seabirds. Mar Ecol Prog Ser 578:117–150Google Scholar
  73. Piatt JF, Sydeman WJ, Wiese F (2007a) Introduction: a modern role for seabirds as indicators. Mar Ecol Prog Ser 352:199–204Google Scholar
  74. Piatt JF, Harding AMA, Shultz M, Speckman SG, Van Pelt TI, Drew GS, Kettle AB (2007b) Seabirds as indicators of marine food supplies: cairns revisited. Mar Ecol Prog Ser 352:221–234Google Scholar
  75. Polito MJ, Trivelpiece WZ, Patterson WP, Karnovsky NJ, Reiss CS, Emslie SD (2015) Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Mar Ecol Prog Ser 519:221–237Google Scholar
  76. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189PubMedGoogle Scholar
  77. 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 103:83–90Google Scholar
  78. Pratte I, Robertson GJ, Mallory ML (2017) Four sympatrically nesting auks show clear resource segregation in their foraging environment. Mar Ecol Prog Ser 572:243–254Google Scholar
  79. Provencher JF, Elliott KH, Gaston AJ, Braune BM (2013) Networks of prey specialization in an Arctic monomorphic seabird. J Avian Biol 44:551–560Google Scholar
  80. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  81. Ramírez I, Paiva VH, Fagundes I, Menezes D, Silva I, Ceia FR, Phillips RA, Ramos JA, Garthe S (2016) Conservation implications of consistent foraging and trophic ecology in a rare petrel species. Anim Conserv 19:139–152Google Scholar
  82. Reed TE, Wanless S, Harris MP, Frederiksen M, Kruuk LEB, Cunningham EJA (2006) Responding to environmental change: plastic responses vary little in a synchronous breeder. Proc Biol Sci 273:2713–2719PubMedPubMedCentralGoogle Scholar
  83. Regular PM, Davoren GK, Hedd A, Montevecchi WA (2010) Crepuscular foraging by a pursuit-diving seabird: tactics of common murres in response to the diel vertical migration of capelin. Mar Ecol Prog Ser 415:295–304Google Scholar
  84. Regular PM, Hedd A, Montevecchi WA, Robertson GJ, Storey AE, Walsh CJ (2014) Why timing is everything: energetic costs and reproductive consequences of resource mismatch for a chick-rearing seabird. Ecosphere 5:155Google Scholar
  85. Rose GA (1998) Acoustic target strength of capelin in Newfoundland waters. ICES J Mar Sci 55:918–923Google Scholar
  86. Scioscia G, Raya Rey A, Saenz Samaniego RA, Florentin O, Schiavini A (2014) Intra- and interannual variation in the diet of the Magellanic penguin (Spheniscus magellanicus) at Martillo Island, Beagle Channel. Polar Biol 37:1421–1433Google Scholar
  87. Shoji A, Elliott K, Fayet A, Boyle D, Perrins C, Guilford T (2015) Foraging behaviour of sympatric razorbills and puffins. Mar Ecol Prog Ser 520:257–267Google Scholar
  88. Stephens DW, Brown JS, Ydenberg RC (2007) Foraging: behavior and ecology. University of Chicago Press, LondonGoogle Scholar
  89. Stock BC, Semmens BX (2016) Unifying error structures in commonly used biotracer mixing models. Ecology 97:576–582Google Scholar
  90. 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(2–4):303–328Google Scholar
  91. Toscano BJ, Gownaris NJ, Heerhartz SM, Monaco CJ (2016) Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecologia 182:55–69PubMedGoogle Scholar
  92. Uttley JD, Walton P, Monaghan P, Austin G (1994) The effects of food abundance on breeding performance and adult time budgets of guillemots Uria aalge. Ibis (Lond 1859) 136:205–213Google Scholar
  93. 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 spots. Ecology 96:3058–3074PubMedGoogle Scholar
  94. 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 13:16–24Google Scholar
  95. Wilhelm SI, Walsh CJ, Storey AE (2008) Time budgets of common murres vary in relation to changes in inshore capelin availability. Condor 110:316–324Google Scholar
  96. Wilhelm SI, Mailhiot J, Arany J, Chardine JW, Robertson GJ, Ryan PC (2015) Update and trends of three important seabird populations in the western North Atlantic using a geographic information system approach. Mar Ornithol 43:211–222Google Scholar
  97. Wilson SK, Burgess SC, Cheal AJ, Emslie M, Fisher R, Miller I, Polunin NVC, Sweatman HPA (2008) Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment. J Anim Ecol 77:220–228PubMedGoogle Scholar
  98. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137Google Scholar
  99. 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 77:1082–1091PubMedGoogle Scholar
  100. Zador SG, Piatt JF (1999) Time-budgets of common murres at a declining and increasing colony in Alaska. Condor 101:149–152Google Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of ManitobaWinnipegCanada

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