Abstract
Foraging differentiation within a species can contribute to restricted gene flow between ecologically different groups, promoting ecological speciation. Galapagos sea lions (Zalophus wollebaeki) show genetic and morphological divergence between the western and central archipelago, possibly as a result of an ecologically mediated contrast in the marine habitat. We use global positioning system (GPS) data, time-depth recordings (TDR), stable isotope and scat data to compare foraging habitat characteristics, diving behaviour and diet composition of Galapagos sea lions from a western and a central colony. We consider both juvenile and adult life stages to assess the potential role of ontogenetic shifts that can be crucial in shaping foraging behaviour and habitat choice for life. We found differences in foraging habitat use, foraging style and diet composition that aligned with genetic differentiation. These differences were consistent between juvenile and adult sea lions from the same colony, overriding age-specific behavioural differences. Our study contributes to an understanding of the complex interaction of ecological condition, plastic behavioural response and genetic make-up of interconnected populations.
Similar content being viewed by others
References
Anthony CD, Venesky MD, Hickerson CM (2008) Ecological separation in a polymorphic terrestrial salamander. J Anim Ecol 77:646–653. doi:10.1111/j.1365-2656.2008.01398.x
Bates Smith T (1987) Bill size polymorphism and intraspecific niche utilization in an African finch. Nature 329:717–719
Bateson P (1981) Ontogeny of behaviour. Br Med Bull 37:159–164
Baylis AMM, Page B, Goldsworthy SD (2008) Colony-specific foraging areas of lactating New Zealand fur seals. Mar Ecol Prog Ser 361:279–290. doi:10.3354/meps07258
Bekkevold D, André C, Dahlgren TG, Clausen LAW, Torstensen E, Mosegaard H, Carvalho GR, Christensen TB, Norlinde E, Ruzzante DE (2005) Environmental correlates of population differentiation in Atlantic herring. Evolution 59:2656–2668
Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519
Chavez FP, Brusca RC (1991) The Galápagos Islands and their relation to oceanographic processes in the tropical Pacific. In: James M (ed) Galápagos marine invertebrates. Plenum, New York, pp 9–33
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. doi:10.1371/journal.pone.0008677
Coyne J, Orr H (2004) Speciation. Sinauer, Sunderland
Davis JM, Stamps JA (2004) The effect of natal experience on habitat preferences. Trends Ecol Evol 19:411–416. doi:10.1016/j.tree.2004.04.006
Dellinger T, Trillmich F (1999) Fish prey of the sympatric Galápagos fur seals and sea lions: seasonal variation and niche separation. Can J Zool 77:1204–1216. doi:10.1139/cjz-77-8-1204
Dobush GR, Ankney CD, Krementz DG (1985) The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Can J Zool 63:1917–1920. doi:10.1139/z85-285
Edgar GJ, Banks S, Fariña JM, Calvopiña M, Martinez C (2004) Regional biogeography of shallow reef fish and macro-invertebrate communities in the Galapagos archipelago. J Biogeogr 80:1107–1124
Feder JL, Flaxman SM, Egan SP, Comeault AA, Nosil P (2013) Geographic mode of speciation and genomic divergence. Annu Rev Ecol Evol Syst 44:73–97. doi:10.1146/annurev-ecolsys-110512-135825
Feldman GC (1984) Patterns of phytoplancton production around the Galápagos Islands. In: Bowman J, Jentsch M, Petersen WT (eds) Tidal mixing and plankton dynamics. Springer, Berlin Heidelberg New York, pp 77–106
Flaxman SM, Wacholder AC, Feder JL, Nosil P (2014) Theoretical models of the influence of genomic architecture on the dynamics of speciation. Mol Ecol 23:4074–4088. doi:10.1111/mec.12750
Ford JKB, Ellis GM, Barrett-Lennard LG, Morton AB, Palm RS, Balcomb KC III (1998) Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can J Zool 76:1456–1471. doi:10.1139/cjz-76-8-1456
Fowler SL, Costa DP, Arnould JPY, Gales NJ, Burns JM (2007a) Ontogeny of oxygen stores and physiological diving capability in Australian sea lions. Funct Ecol 21:922–935. doi:10.1111/j.1365-2435.2007.01295.x
Fowler SL, Costa DP, Arnould JPY (2007b) Ontogeny of movements and foraging ranges in the Australian sea lion. Mar Mammal Sci 23:598–614. doi:10.1111/j.1748-7692.2007.00134.x
Götz KT, Robinson PW, Hobbs RC, Laidre KL, Huckstadt LA, Shelden KEW (2012) Movement and dive behaviour of beluga whales in Cook Inlet, Alaska. AFSC processed report 2012-03. AFSC, Seattle, WA
Halsey LG, Blackburn TM, Butler PJ (2006a) A comparative analysis of the diving behaviour of birds and mammals. Funct Ecol 20:889–899. doi:10.1111/j.1365-2435.2006.01170.x
Halsey LG, Butler PJ, Blackburn TM (2006b) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287. doi:10.1086/499439
Hendry AP (2004) Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol Ecol Res 6:1219–1236
Hoffman JI, Forcada J (2012) Extreme natal philopatry in female Antarctic fur seals (Arctocephalus gazella). Mamm Biol 77:71–73. doi:10.1016/j.mambio.2011.09.002
Hoffman JI, Steinfartz S, Wolf JBW (2007) Ten novel dinucleotide microsatellite loci cloned from the Galápagos sea lion (Zalophus californianus wollebaeki) are polymorphic in other pinniped species. Mol Ecol Notes 7:103–105
Jeglinski JWE, Mueller B, Pörschmann U, Trillmich F (2010) Field-based age estimation of juvenile Galapagos sea lions (Zalophus wollebaeki) using morphometric measurements. Aquat Mamm 36:262–269. doi:10.1578/AM.36.3.2010.262
Jeglinski JWE, Robinson PW, Werner C, Costa DP, Trillmich F (2012) Age, body mass and environmental variation shape the foraging ontogeny of Galapagos sea lions. Mar Ecol Prog Ser 453:279–296
Jeglinski JWE, Goetz KT, Werner C, Costa DP, Trillmich F (2013) Same size–same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. J Anim Ecol 82:694–706. doi:10.1111/1365-2656.12019
Kernohan BJ, Gitzen RA, Millspaugh JJ (2001) Analysis of animal space use and movements. In: Millspaugh JJ, Marzluff JM (eds) Radio tracking animal populations. Academic Press, San Diego, pp 125–166
Kie JG, Matthiopoulos J, Fieberg J, Powell RA, Cagnacci F, Mitchell MS, Gaillard J-M, Moorcroft PR (2010) The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philos Trans R Soc B Biol Sci 365:2221–2231. doi:10.1098/rstb.2010.0093
Krutzen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB (2005) Cultural transmission of tool use in bottlenose dolphins. Proc Natl Acad Sci 102:5
Kuhn CE, McDonald BI, Shaffer SA, Barnes J, Crocker DE, Burnes J, Costa DP (2006) Diving physiology and winter foraging behavior of a juvenile leopard seal (Hydrurga leptonyx). Polar Biol 29:303–307. doi:10.1007/s00300-005-0053-x
Kurle CM, Worthy GAJ (2002) Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Mar Ecol Prog Ser 236:289–300. doi:10.3354/meps236289
Lewis R, O’Connell TC, Lewis M et al (2006) Sex-specific foraging strategies and resource partitioning in the southern elephant seal (Mirounga leonina). Proc R Soc Lond B Biol 273:2901–2907. doi:10.1098/rspb.2006.3642
Louis M, Fontaine MC, Spitz J, Schlund E, Dabin W, Deaville R, Caurant F, Cherel Y, Guinet C, Simon-Bouhet B (2014) Ecological opportunities and specializations shaped genetic divergence in a highly mobile marine top predator. Proc R Soc Lond B Biol 281:20141558. doi:10.1098/rspb.2014.1558
Lowther AD, Goldsworthy SD (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
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
Meise K, Krüger O, Piedrahita P, Trillmich F (2013) Site fidelity of male Galápagos sea lions: a lifetime perspective. Behav Ecol Sociobiol 67:1001–1011. doi:10.1007/s00265-013-1526-5
Morin PA, Archer FI, Foote AD et al (2008) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20:908–916. doi:10.1101/gr.102954.109.908
Mueller B, Pörschmann U, Wolf JBW, Trillmich F (2011) Growth under uncertainty: the influence of marine variability on early development of Galapagos sea lions. Mar Mammal Sci 27:350–365. doi:10.1111/j.1748-7692.2010.00404.x
Olsson J, Quevedo M, Colson C, Svanbäck R (2007) Gut length plasticity in perch: into the bowels of resource polymorphisms. Biol J Linn Soc 90:517–523
Páez-Rosas D, Aurioles-Gamboa D (2010) Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki. Mar Biol 157:2769–2781. doi:10.1007/s00227-010-1535-0
Peck DR, Congdon BC (2005) Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus. Mar Ecol Prog Ser 299:289–296
Peters A, Hothorn T (2015) Ipred: improved predictors. R package version 0.9-5. http://CRAN.R-project.org/package=ipred
Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci 71:2141–2145
Pörschmann U, Trillmich F, Mueller B, Wolf JBW (2010) Male reproductive success and its behavioural correlates in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki). Mol Ecol 19:2574–2586. doi:10.1111/j.1365-294X.2010.04665.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Riesch R, Barrett-Lennard LG, Ellis GM, Ford JKB, Deecke V (2012) Cultural traditions and the evolution of reproductive isolation: ecological speciation in killer whales? Biol J Linn Soc 106:1–17. doi:10.1111/j.1095-8312.2012.01872.x
Robinson PW, Villegas-Amtmann S, Costa DP (2009) Field validation of an inexpensive time-depth recorder. Mar Mammal Sci 25:199–205. doi:10.1111/j.1748-7692.2008.00227.x
Ruckstuhl KE (2007) Sexual segregation in vertebrates: proximate and ultimate causes. Integr Comp Biol 47:245–257. doi:10.1093/icb/icm030
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi:10.1111/j.1461-0248.2004.00715.x
Salazar-Pico S, Bustamante R (2003) Effects of the 1997–1998 El Nino on population size and diet of the Galapagos sea lion (Zalophus wollebaeki). Not Galapagos 62:40–45
Schaeffer BA, Morrison JM, Kamykowski D, Feldman GC, Xie L, Liu Y, Sweet W, McCulloch A, Banks S (2008) Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine Reserve by MODIS, a surface acquisition system, and in situ measurements. Remote Sens Environ 112:3044–3054. doi:10.1016/j.rse.2008.03.005
Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380
Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358. doi:10.1139/z97-044
Selonen V, Hanski IK, Desrochers A (2007) Natal habitat-biased dispersal in the Siberian flying squirrel. Proc R Soc Lond 274:2063–2068. doi:10.1098/rspb.2007.0570
Shafer ABA, Wolf JBW (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecol Lett 16:940–950. doi:10.1111/ele.12120
Shannon C (1948) A mathematical theory of communication. Bell Syst Tech J 3:379–423
Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370
Slagsvold T, Wiebe KL (2007) Learning the ecological niche. Proc R Soc Lond B Biol 274:19–23. doi:10.1098/rspb.2006.3663
Slagsvold T, Wiebe KL (2011) Social learning in birds and its role in shaping a foraging niche. Philos Trans R Soc B Biol Sci 366:969–977. doi:10.1098/rstb.2010.0343
Smith TB, Skulason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians and birds. Annu Rev Ecol Syst 27:111–133
Spence-Bailey LM, Verrier D, Arnould JPY (2007) The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups. J Comp Physiol B 177:483–494. doi:10.1007/s00360-007-0146-7
Stamps JA, Davis JM (2006) Adaptive effects of natal experience on habitat selection by dispersers. Anim Behav 72:1279–1289. doi:10.1016/j.anbehav.2006.03.010
Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci 105:560–565. doi:10.1073/pnas.0709263105
Tremblay Y, Shaffer S, Fowler SL, Kuhn CE, McDonald BI, Weise MJ, Bost C-A, Weimerskirch H, Crocker DE, Goebel ME, Costa DP (2006) Interpolation of animal tracking data in a fluid environment. J Exp Biol 209:128–140. doi:10.1242/jeb.01970
Trillmich F (1990) The behavioural ecology of maternal effort in fur seals and sea lions. Behaviour 114:1–4
Trillmich F, Wolf JBW (2008) Parent–offspring and sibling conflict in Galápagos fur seals and sea lions. Behav Ecol Sociobiol 62:363–375. doi:10.1007/s00265-007-0423-1
Villegas-Amtmann S, Costa DP (2010) Oxygen stores plasticity linked to foraging behaviour and pregnancy in a diving predator, the Galapagos sea lion. Funct Ecol 24:785–795. doi:10.1111/j.1365-2435.2009.01685.x
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. doi:10.3354/meps07457
Weihs C, Ligges U, Luebke K, Raabe N (2005) klaR analyzing German business cycles. In: Baier D, Decker R, Schmidt-Thieme L (eds) Data analysis and decision support. Springer Heidelberg New York, Berlin, pp 335–343
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425. doi:10.1146/annurev.es.15.110184.002141
Wolf JBW, Trillmich F (2007) Beyond habitat requirements: individual fine-scale site fidelity in a colony of the Galapagos sea lion (Zalophus wollebaeki) creates conditions for social structuring. Behav Ecol 152:553–567. doi:10.1007/s00442-007-0665-7
Wolf JBW, Tautz D, Caccone A, Steinfartz S (2006) Development of new microsatellite loci and evaluation of loci from other pinniped species for the Galapagos sea lion (Zalophus californianus wollebaeki). Conserv Genet 7:461–465. doi:10.1007/s10592-005-9045-1
Wolf JBW, 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 13:1–13. doi:10.1186/1742-9994-4-20
Wolf JBW, Harrod C, Brunner S, Salazar S, Trillmich F, Tautz D (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations. BMC Evol Biol 8:150. doi:10.1186/1471-2148-8-150
Zuur AF, Ieno EN, Walker NJ, Savliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. doi:10.1007/978-0-387-87458-6
Acknowledgments
The present study was performed under the permit nos. PC-11-08 and PC-043-09 of the National Park Service, Galapagos and financed by the German Science Foundation (grant TR 105/19-1) and National Geographic (grant no. 8682-09). We received highly appreciated material sponsorship by Panasonic, Ortlieb, Zarges and Huntsmann Advanced Materials. The Charles Darwin Research Station and the National Park Service provided logistic support during fieldwork. We thank David Anchundia, Enzo Garcia Bartholomei, Paddy Brock, Valentina Francu-Trecu, Melinda Fowler, Matthias Marquardt, Gitte MacDonald, Sara Maxwell, Manuel Meija, Birte Müller, Diego Paéz-Rosas, Patrick Robinson, Maria Szphegyi, Michael Tift and Stella Villegas-Amtmann for their help in the field. Stephanie Kramer-Schadt gave helpful advice on data processing, Barbara Teichner and Elke Hippauf helped with lab work, Kristine Meise helped with genetic data processing and Andrea Florez sorted the OTs. Mark S. Lowry, Southwest Fisheries Science Center, National Marine Fisheries Service, National Atmospheric Administration, identified the otoliths using the John Fitch Otolith Collection at the Los Angeles County Museum of Natural History, Los Angeles, California. Judy Stamps, Julien Claude and three anonymous referees provided helpful comments on an earlier version of the manuscript. This publication is contribution no. 2121 of the Charles Darwin Foundation for the Galapagos Islands.
Author contribution statement
F. T. and J. B. W. W. formulated the original idea and F. T. and J. W. E. J. designed the study. J. W. E. J., F. T. and D. P. C. collected the data, J. W. E. J. analysed the data, with support from C. W. for stable isotope lab work and from J. B. W. W. for genetic data analysis. J. W. E. J. wrote the manuscript and other authors provided editorial advice.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jörg U. Ganzhorn.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jeglinski, J.W.E., Wolf, J.B.W., Werner, C. et al. Differences in foraging ecology align with genetically divergent ecotypes of a highly mobile marine top predator. Oecologia 179, 1041–1052 (2015). https://doi.org/10.1007/s00442-015-3424-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-015-3424-1