Skip to main content

Advertisement

SpringerLink
Log in

Foraging strategies of a generalist marine predator inhabiting a dynamic environment

  • Behavioral ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Intraspecific variability is increasingly recognized as an important component of foraging behavior that can have implications for both population and community dynamics. We used an individual-level approach to describe the foraging behavior of an abundant, generalist predator that inhabits a dynamic marine ecosystem, focusing specifically on the different foraging strategies used by individuals in the same demographic group. We collected data on movements and diving behavior of adult female California sea lions (Zalophus californianus) across multiple foraging trips to sea. Sea lions (n = 35) used one of three foraging strategies that primarily differed in their oceanic zone and dive depth: a shallow, epipelagic strategy, a mixed epipelagic/benthic strategy, and a deep-diving strategy. Individuals varied in their degree of fidelity to a given strategy, with 66 % of sea lions using only one strategy on all or most of their foraging trips across the two-month tracking period. All foraging strategies were present in each of the sampling years, but there were inter-annual differences in the population-level importance of each strategy that may reflect changes in prey availability. Deep-diving sea lions traveled shorter distances and spent a greater proportion of time at the rookery than sea lions using the other two strategies, which may have energetic and reproductive implications. These results highlight the importance of an individual-based approach in describing the foraging behavior of female California sea lions and understanding how they respond to the seasonal and annual changes in prey availability that characterize the California Current System.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Antonelis GA, Stewart BS, Perryman WF (1990) Foraging characteristics of female northern fur seals (Callorhinus ursinus) and California sea lions (Zalophus californianus). Can J Zool 68:150–158. doi:10.1139/z90-022

    Article  Google Scholar 

  • Araújo MS, Martins EG, Cruz LD et al (2010) Nested diets: a novel pattern of individual-level resource use. Oikos 119:81–88. doi:10.1111/j.1600-0706.2009.17624.x

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Arnould JPY, Boyd IL (1995) Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). J Zool Lond 237:1–12

    Article  Google Scholar 

  • Arnould JP, Hindell MA (1999) The composition of Australian fur seal (Arctocephalus pusillus doriferus) milk throughout lactation. Physiol Biochem Zool 72:605–612. doi:10.1086/316702

    Article  CAS  PubMed  Google Scholar 

  • Arnould JPY, Hindell MA (2001) Dive behaviour, foraging locations, and maternal-attendance patterns of Australian fur seals (Arctocephalus pusillus doriferus). Can J Zool 79:35–48. doi:10.1139/cjz-79-1-35

    Article  Google Scholar 

  • Arnould J, Boyd IL, Speakman JR (1996) The relationship between foraging behavior and energy expenditure in Antarctic fur seals. J Zool Soc Lond 239:769–782

    Article  Google Scholar 

  • Augé AA, Chilvers BL, Moore AB, Davis LS (2014) Importance of studying foraging site fidelity for spatial conservation measures in a mobile predator. Anim Conserv 17:61–71. doi:10.1111/acv.12056

    Article  Google Scholar 

  • Baylis AMM, Orben RA, Arnould JPY et al (2015) Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia 179:1053–1065. doi:10.10007/s00442-015-3421-4

    Article  CAS  PubMed  Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi:10.1086/343878

    Article  PubMed  Google Scholar 

  • Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192. doi:10.1016/j.tree.2011.01.009

    Article  PubMed  PubMed Central  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 63:703–713

    Article  Google Scholar 

  • Buckley TW, Livingston PA (1997) Geographic variation in the diet of Pacific hake, with a note on cannibalism. Calif Coop Ocean Fish Investig Rep 38:53–62

    Google Scholar 

  • Cantor M, Pires MM, Longo GO et al (2013) Individual variation in resource use by opossums leading to nested fruit consumption. Oikos 122:1085–1093. doi:10.1111/j.1600-0706.2012.00070.x

    Article  Google Scholar 

  • Carretta J V, Oleson EM, Weller DW, et al (2015) US Pacific marine mammal stock assessments: 2014. NOAA-TM-NMFS-SWFSC-549. doi: 10.7289/V5/TM-SWFSC-549

  • Ceia FR, Ramos JA (2015) Individual specialization in the foraging and feeding strategies of seabirds: a review. Mar Biol. doi:10.1007/s00227-015-2735-4

    Google Scholar 

  • Checkley DM, Barth JA (2009) Patterns and processes in the California Current System. Prog Oceanogr 83:49–64. doi:10.1016/j.pocean.2009.07.028

    Article  Google Scholar 

  • Cherel Y, Hobson K (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. doi:10.3354/meps329281

    Article  CAS  Google Scholar 

  • Chilvers B, Wilkinson I (2009) Diverse foraging strategies in lactating New Zealand sea lions. Mar Ecol Prog Ser 378:299–308. doi:10.3354/meps07846

    Article  Google Scholar 

  • Costa DP, Gales NJ (2000) Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. J Exp Biol 203:3655–3665

    CAS  PubMed  Google Scholar 

  • Costa DP, Gentry RL (1986) Reproductive energetics of northern fur seals. In: Gentry RL, Kooyman GL (eds) Fur seals: maternal strategies on land and at sea. Princeton University Press, Princeton, New Jersey, pp 79–101

    Google Scholar 

  • Costa DP, Kuhn CE, Weise MJ et al (2004) When does physiology limit the foraging behaviour of freely diving mammals? Int Congr Ser 1275:359–366. doi:10.1016/j.ics.2004.08.058

    Article  Google Scholar 

  • Costa DP, Robinson PW, Arnould JPY et al (2010) Accuracy of ARGOS locations of pinnipeds at-sea estimated using Fastloc GPS. PLoS One 5:e8677. doi:10.1371/journal.pone.0008677

    Article  PubMed  PubMed Central  Google Scholar 

  • Feldkamp SD, DeLong RL, Antonelis GA (1989) Diving patterns of California sea lions, Zalophus californianus. Can J Zool 67:872–883. doi:10.1139/z89-129

    Article  Google Scholar 

  • Goldsworthy SD (2006) Maternal strategies of the New Zealand fur seal: evidence for interannual variability in provisioning and pup growth strategies. Aust J Zool 54:31–44. doi:10.1071/ZO05041

    Article  Google Scholar 

  • Hare SR, Mantua NJ (2000) Empirical evidence for North Pacific regime shifts in 1977 and 1989. Prog Oceanogr 47:103–145. doi:10.1016/S0079-6611(00)00033-1

    Article  Google Scholar 

  • Harris JD (2016) Estimation of an unobservable transition: from dependence to weaning in the California sea lion (Zalophus californianus). Master thesis, School of Environmental and Forest Sciences, University of Washington, Seattle, WA, USA. doi:10.1017/CBO9781107415324.004

  • Hoskins AJ, Costa DP, Wheatley KE et al (2015) Influence of intrinsic variation on foraging behaviour of adult female Australian fur seals. Mar Ecol Prog Ser 526:227–239. doi:10.3354/meps11200

    Article  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi:10.1111/j.1461-0248.2008.01179.x

    Article  PubMed  Google Scholar 

  • Huynh MD, Kitts DD (2009) Evaluating nutritional quality of pacific fish species from fatty acid signatures. Food Chem 114:912–918. doi:10.1016/j.foodchem.2008.10.038

    Article  CAS  Google Scholar 

  • Kernaléguen L, Cazelles B, Arnould JPY et al (2012) Long-term species, sexual and individual variations in foraging strategies of fur seals revealed by stable isotopes in whiskers. PLoS One 7:e32916. doi:10.1371/journal.pone.0032916

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 84:1081–1091. doi:10.1111/1365-2656.12347

    Article  PubMed  Google Scholar 

  • Kernaléguen L, Dorville N, Ierodiaconou D et al (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. doi:10.1007/s00442-015-3407-2

    Article  PubMed  Google Scholar 

  • Killen SS, Marras S, Mckenzie DJ (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. J Anim Ecol 80:1024–1033. doi:10.1111/j.1365-2656.2011.01844.x

    Article  PubMed  Google Scholar 

  • Kuhn CE, Costa DP (2014) Interannual variation in the at-sea behavior of California sea lions (Zalophus californianus). Mar Mammal Sci 30:1297–1319. doi:10.1111/mms.12110

    Article  Google Scholar 

  • Kuhn C, Tremblay Y, Ream R, Gelatt T (2010) Coupling GPS tracking with dive behavior to examine the relationship between foraging strategy and fine-scale movements of northern fur seals. Endanger Species Res 12:125–139. doi:10.3354/esr00297

    Article  Google Scholar 

  • Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

    Article  Google Scholar 

  • Leising AW, Schroeder ID, Bograd SJ et al (2014) State of the California Current 2013-14: El Niño looming. Calif Coop Ocean Fish Investig Rep 55:51–87

    Google Scholar 

  • Litz MNC, Brodeur RD, Emmett RL et al (2010) Effects of variable oceanographic conditions on forage fish lipid content and fatty acid composition in the northern California Current. Mar Ecol Prog Ser 405:71–85. doi:10.3354/meps08479

    Article  CAS  Google Scholar 

  • Livingston PA (1983) Food habitat of Pacific whiting, Merluccius productus, off the west coast of North America, 1967 and 1980. Fish Bull 81:629–636

    Google Scholar 

  • Lowry MS, Stewart BS, Heath CB et al (1988) Seasonal and annual variability in the diet of California sea lions Zalophus californianus at San Nicolas Island, California, 1981-86. Fish Bull 89:331–336

    Google Scholar 

  • Lowther A, Goldsworthy S (2011) Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) colonies using stable isotope analysis. Mar Mammal Sci 27:567–586. doi:10.1111/j.1748-7692.2010.00425.x

    Article  Google Scholar 

  • 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. doi:10.3354/meps09392

    Article  Google Scholar 

  • Lowther AD, Harcourt RG, Goldsworthy SD, Stow A (2012) Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity. Anim Behav 83:691–701. doi:10.1016/j.anbehav.2011.12.015

    Article  Google Scholar 

  • McClatchie S, Field J, Thompson AR et al (2016) Food limitation of sea lion pups and the decline of forage off central and southern California. R Soc Open Sci 3:150628. doi:10.1098/rsos.150628

    Article  PubMed  PubMed Central  Google Scholar 

  • McGowan JA, Bograd SJ, Lynn RJ, Miller AJ (2003) The biological response to the 1977 regime shift in the California Current. Deep Sea Res Part II Top Stud Oceanogr 50:2567–2582. doi:10.1016/S0967-0645(03)00135-8

    Article  Google Scholar 

  • Melin SR, Delong RL, Thomason JR, VanBlaricom GR (2000) Attendance patterns of California sea lion (Zalophus californianus) females and pups during the non-breeding season at San Miguel Island. Mar Mammal Sci 16:169–185

    Article  Google Scholar 

  • 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. doi:10.1139/Z07-132

    Article  Google Scholar 

  • Melin SR, Orr AJ, Harris JD, Delong RL (2012) California sea lions: an indicator for integrated ecosystem assessment of the California Current System. Calif Coop Ocean Fish Investig Rep 53:140–152

    Google Scholar 

  • Newsome SD, Tinker MT, Gill VA et al (2015) The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters. Oecologia 178:45–59. doi:10.1007/s00442-015-3223-8

    Article  PubMed  Google Scholar 

  • Ono KA, Boness DJ, Oftedal OT (1985) The effect of a natural environmental disturbance on maternal investment and pup behavior in the California sea lion. Behav Ecol Sociobiol 21:109–118

    Article  Google Scholar 

  • Orr A, VanBlaricom G, DeLong R et al (2011) Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses. Can J Zool 89:109–122. doi:10.1139/Z10-101

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Rayner MJ, Hartill BW, Hauber ME, Phillips RA (2010) Central place foraging by breeding Cook’s petrel Pterodroma cookii: foraging duration reflects range, diet and chick meal mass. Mar Biol 157:2187–2194. doi:10.1007/s00227-010-1483-8

    Article  Google Scholar 

  • Rosenblatt AE, Nifong JC, Heithaus MR et al (2015) Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178:5–16. doi:10.1007/s00442-014-3201-6

    Article  PubMed  Google Scholar 

  • Schreer JF, Kovacs KM, O’Hara Hines RJ (2001) Comparative diving patterns of pinnipeds and seabirds. Ecol Monogr 71:137–162. doi:10.1890/0012-9615(2001)071[0137:CDPOPA]2.0.CO;2

    Article  Google Scholar 

  • Staniland IJ, Boyd IL, Reid K (2007) An energy-distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella). Mar Biol 152:233–241. doi:10.1007/s00227-007-0698-9

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tinker M, Guimarães PR, Novak M et al (2012) Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters. Ecol Lett 15:475–483. doi:10.1111/j.1461-0248.2012.01760.x

    Article  Google Scholar 

  • Tremblay Y, Cherel Y (2000) Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Mar Ecol Prog Ser 204:257–267

    Article  Google Scholar 

  • Villegas-Amtmann S, Costa D, Tremblay Y et al (2008) Multiple foraging strategies in a marine apex predator, the Galapagos sea lion Zalophus wollebaeki. Mar Ecol Prog Ser 363:299–309. doi:10.3354/meps07457

    Article  Google Scholar 

  • Villegas-Amtmann S, Simmons SE, Kuhn CE et al (2011) Latitudinal range influences the seasonal variation in the foraging behavior of marine top predators. PLoS One 6:e23166. doi:10.1371/journal.pone.0023166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villegas-Amtmann S, Jeglinski JWE, Costa DP et al (2013) Individual foraging strategies reveal niche overlap between endangered Galapagos pinnipeds. PLoS One 8:e70748. doi:10.1371/journal.pone.0070748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. doi:10.1016/j.tree.2011.11.014

    Article  PubMed  Google Scholar 

  • Weise M, Harvey JT (2008) Temporal variability in ocean climate and California sea lion diet and biomass consumption: implications for fisheries management. Mar Ecol Prog Ser 373:157–172. doi:10.3354/meps07737

    Article  Google Scholar 

  • Weise MJ, Harvey JT, Costa DP (2010) The role of body size in individual-based foraging strategies of a top marine predator. Ecology 91:1004–1015

    Article  PubMed  Google Scholar 

  • Wolf JB, Tautz D, Trillmich F (2007) Galápagos and Californian sea lions are separate species: genetic analysis of the genus Zalophus and its implications for conservation management. Front Zool 4:20. doi:10.1186/1742-9994-4-20

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeidberg LD, Butler JL, Ramon D et al (2012) Estimation of spawning habitats of market squid (Doryteuthis opalescens) from field surveys of eggs off Central and Southern California. Mar Ecol 33:326–336. doi:10.1111/j.1439-0485.2011.00498.x

    Article  Google Scholar 

Download references

Acknowledgments

We thank Seth Newsome for helpful suggestions that improved the quality of this manuscript, the US. Navy for logistical support, and all of the field volunteers, without which this research would not have been possible. Data collection was part of the Tagging of Pelagic Predators (TOPP) project, and funded by the California Sea Grant Program, National Oceanographic Partnership Program, the Office of Naval Research, and the Moore, Packard, and Sloan Foundations. EAM was supported on a grant from the E & P Sound and Marine Life Joint Industry Programme (#22 07–23). Animal handling was permitted under NMFS permit #87-1593, 1851 and approved by the University of California Santa Cruz Institutional Animal Care and Use Committee.

Author contribution statement

EAM and DPC conceived the study, DPC, PWR, SES, CEK, and MF lead fieldwork, EAM and PWR analyzed the data, EAM wrote the manuscript, with contributions from all authors.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, 95064, USA

    E. A. McHuron, P. W. Robinson & D. P. Costa

  2. Marine Mammal Commission, Bethesda, MD, 20814, USA

    S. E. Simmons

  3. National Marine Mammal Laboratory, Alaska Fisheries Science Center/NOAA, Seattle, WA, 98115, USA

    C. E. Kuhn

  4. Springfield College, Springfield, MA, 01109, USA

    M. Fowler

Authors
  1. E. A. McHuron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. W. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. E. Simmons
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. E. Kuhn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Fowler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. P. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. McHuron.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Hannu J. Ylonen.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McHuron, E.A., Robinson, P.W., Simmons, S.E. et al. Foraging strategies of a generalist marine predator inhabiting a dynamic environment. Oecologia 182, 995–1005 (2016). https://doi.org/10.1007/s00442-016-3732-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3732-0

Keywords

Search

Navigation