Constrained by consistency? Repeatability of foraging behavior at multiple timescales for a generalist marine predator
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.
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.
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
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.
- Arnould J, Boyd IL, Speakman JR (1996) The relationship between foraging behavior and energy expenditure in Antarctic fur seals. J Zool Soc Lond 239:769–782Google Scholar
- 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 Google Scholar
- Boyd IL, Arnould JPY, Barton T, Croxall JP (1994) Foraging behavior of Antarctic fur seals during periods of contrasting prey abundance. J Anim Ecol 63:703–713Google Scholar
- 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
- 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 578:151–166Google Scholar
- Costa DP, Croxall JP, Duck CD (1989) Foraging energetics of Antarctic fur seals in relation to changes in prey availability. Ecology 70:596–606Google Scholar
- 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 PubMedPubMedCentralGoogle Scholar
- Duong T (2018) ks: Kernel smoothing. R package version 1.11.0. https://CRAN.R-project.org/package=ks
- Fieberg J, Kochanny CO (2005) Quantifying home-range overlap: the importance of the utilization distribution. J Wildl Manag 69:1346–1359Google Scholar
- 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 Google Scholar
- 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 Google Scholar
- 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 PubMedPubMedCentralGoogle Scholar
- 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 PubMedGoogle Scholar
- Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18Google Scholar
- 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
- 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
- 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 567:235–247Google Scholar
- Mori Y, Boyd IL (2004) The behavioral basis for nonlinear functional responses and optimal foraging in Antarctic fur seals. Ecology 85:398–410Google 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. https://doi.org/10.1111/j.1600-0706.2013.00406.x Google Scholar
- 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 Google Scholar
- 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 PubMedGoogle Scholar
- 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
- 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 Google Scholar
- R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
- 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 Google Scholar
- 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 Google Scholar
- 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 Google Scholar