Differences in foraging ecology align with genetically divergent ecotypes of a highly mobile marine top predator

Oecologia

Volumn 179, Issue 4, 2015, Pages 1041-1052

  Jeglinski, Jana W E ^a,f   Wolf, Jochen B W ^b   Werner, Christiane ^c,d   Costa, Daniel P ^e   Trillmich, Fritz ^f  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF BAYREUTH   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BIELEFELD UNIVERSITY   (Germany)

Author keywords

Biologging; Early learning; Genetic differentiation; Ontogeny; Zalophus wollebaeki

Indexed keywords

ARCHIPELAGO; DIET; ECOTYPE; FORAGING BEHAVIOR; GENE FLOW; GENETIC DIFFERENTIATION; GPS; HABITAT SELECTION; JUVENILE; ONTOGENY; PINNIPED; PREDATOR; SPECIATION (BIOLOGY); TOP-DOWN CONTROL;

OTARIIDAE; ZALOPHUS WOLLEBAEKI;

ACCLIMATIZATION; ANIMAL; ANIMAL BEHAVIOR; DIET; ECOLOGY; ECOSYSTEM; ECOTYPE; EVOLUTION; FEEDING BEHAVIOR; GENE FLOW; GENETIC DRIFT; GENETICS; OTARIIDAE; PHENOTYPE; PHYSIOLOGY; PREDATION;

ACCLIMATIZATION; ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; DIET; ECOLOGY; ECOSYSTEM; ECOTYPE; FEEDING BEHAVIOR; GENE FLOW; GENETIC DRIFT; PHENOTYPE; PREDATORY BEHAVIOR; SEA LIONS;

EID: 84946490468     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-015-3424-1     Document Type: Article

References (77)

1. 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
2. Bates Smith T (1987) Bill size polymorphism and intraspecific niche utilization in an African finch. Nature 329:717–719
3. Bateson P (1981) Ontogeny of behaviour. Br Med Bull 37:159–164
4. 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
5. 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
6. 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
7. 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
8. 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
9. Coyne J, Orr H (2004) Speciation. Sinauer, Sunderland
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. 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
22. Halsey LG, Butler PJ, Blackburn TM (2006b) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287. doi:10.1086/499439
23. Hendry AP (2004) Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol Ecol Res 6:1219–1236
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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
38. 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
39. 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
40. 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
41. 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
42. 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
43. 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
44. Peters A, Hothorn T (2015) Ipred: improved predictors. R package version 0.9-5. http://CRAN.R-project.org/package=ipred
45. Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci 71:2141–2145
46. 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
47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
48. 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
49. 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
50. Ruckstuhl KE (2007) Sexual segregation in vertebrates: proximate and ultimate causes. Integr Comp Biol 47:245–257. doi:10.1093/icb/icm030
51. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi:10.1111/j.1461-0248.2004.00715.x
52. 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
53. 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
54. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380
55. Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358. doi:10.1139/z97-044
56. 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
57. 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
58. Shannon C (1948) A mathematical theory of communication. Bell Syst Tech J 3:379–423
59. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370
60. Slagsvold T, Wiebe KL (2007) Learning the ecological niche. Proc R Soc Lond B Biol 274:19–23. doi:10.1098/rspb.2006.3663
61. 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
62. Smith TB, Skulason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians and birds. Annu Rev Ecol Syst 27:111–133
63. 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
64. 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
65. 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
66. 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
67. Trillmich F (1990) The behavioural ecology of maternal effort in fur seals and sea lions. Behaviour 114:1–4
68. 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
69. 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
70. 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
71. 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
72. 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
73. 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
74. 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
75. 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
76. 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
77. 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