Advertisement

Marine Biology

, Volume 156, Issue 7, pp 1375–1387 | Cite as

Phylogeography of California and Galápagos sea lions and population structure within the California sea lion

  • Yolanda Schramm
  • S. L. Mesnick
  • J. de la Rosa
  • D. M. Palacios
  • M. S. Lowry
  • D. Aurioles-Gamboa
  • H. M. Snell
  • S. Escorza-Treviño
Original Paper

Abstract

We investigate the phylogeography of California (Zalophus californianus) and Galápagos (Z. wollebaeki) sea lions and describe within-population structure for the California sea lion based on mitochondrial DNA. Fifty control-region haplotypes were found, 41 from Z. californianus and 9 from Z. wollebaeki, with three fixed differences between the two species. Ranked population boundaries along the range of Z. californianus were defined based on the Monmonier Maximum Difference Algorithm, resulting in five genetically distinct populations, two in the Pacific Ocean and three inside the Gulf of California. A Minimum Spanning Network showed a strong phylogeographic signal with two well-defined clusters, Z. californianus and Z. wollebaeki, separated by six base-pair differences, supporting the existence of two genetically distinct species with an estimated divergence time of ~0.8 Ma. Results are discussed in the context of the historical geologic and paleoceanographic events of the last 1 Ma in the eastern Pacific.

Keywords

Leptospirosis Pacific Population Pacific Temperate Minimum Span Network Tooth Erosion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Tissue samples were collected in México under permit No. DOO750.8106-97 from the Instituto Nacional de Ecología; in California under permit No. 1026 from the US Department of Commerce; and in Galápagos, Ecuador, under permit No. PC-009-99 from the Galápagos National Park (and permit No. 017-00 for sample export). Additional sea lion samples from San Miguel Island were kindly provided by S. Melin (US National Marine Fisheries Service) and from Galápagos by S.K. Salazar (Charles Darwin Research Station). Work in México was facilitated by A. Zavala and O. Maravilla and carried out on Mexican Navy ships. G. Heckel, L. Inclán and M.L. Anoge participated during the cruise. We acknowledge the invaluable logistical support provided by the Charles Darwin Research Station in Galápagos (through P. Robayo). Thanks to the welcome provided by A. Dizon and staff at the SWFSC Marine Mammal Genetics Laboratory and to C. Le Duc, K. Robertson and J. Hyde for their assistance in the lab. Y.S. had grants from the Mexican National Science Foundation (CONACyT), Alstom Power (Rosarito, México), and the Universidad Autónoma de Baja California. D.M.P. was supported by award No. N00014-05-1-0045 from the US Office of Naval Research, National Oceanographic Partnership Program. Supplemental funding for Galápagos sample export was provided by the Protected Resources Division of the SWFSC (through R.L. Brownell Jr.). Earlier drafts of the manuscript benefited from comments by G. Heckel. We thank to two anonymous reviewers for their valuable suggestions and comments. The experiments comply with the current laws of the USA, México and Ecuador.

References

  1. Acevedo-Whitehouse K, de la Cueva H, Gulland FMD, Aurioles-Gamboa D, Arellano-Carbajal F, Suárez-Guemes F (2003) Evidence of Leptospira interrogans infection in California sea lion pups from the Gulf of California. J Wildl Dis 39:145–151CrossRefGoogle Scholar
  2. Acevedo-Whitehouse K, Spraker TR, Lyons E, Melin SR, Gulland F, Delong RL, Amos W (2006) Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol Ecol 15:1973–1982. doi: https://doi.org/10.1111/j.1365-294X.2006.02903.x CrossRefGoogle Scholar
  3. Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galápagos penguin and the Magellanic penguin. Cons Gen 3:375–383. doi: https://doi.org/10.1023/A:1020555303124 CrossRefGoogle Scholar
  4. Amos B, Hoelzel AR (1991) Long-term preservation of whale skin for DNA analysis. In: Hoelzel AR (ed) The genetic ecology of whales and dolphins. Special publication no. 13 of the IWC, Cambridge, pp 99–103Google Scholar
  5. Antonelis GA, Stewart BS, Perryman WS (1990) Foraging characteristics of female northern fur seals (Callorhinus ursinus) and California sea lions (Zalophus californianus). Can J Zool 68:150–158. doi: https://doi.org/10.1139/z90-022 CrossRefGoogle Scholar
  6. Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34:493–505. doi: https://doi.org/10.1007/BF00160463 CrossRefGoogle Scholar
  7. Aurioles-Gamboa D, Díaz-Guzmán C, Le Boeuf BJ, Casper D (2009) Temporomandibular arthritis and osteomielitis in California sea lions (Zalophus califorinianus). J Zoo Wildl Med (in press)Google Scholar
  8. Aurioles-Gamboa D, Le Boeuf BJ (1991) Effects of the El Niño 1982–1983 on California Sea Lions in México. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 112–118CrossRefGoogle Scholar
  9. Aurioles-Gamboa D, Zavala-González A (1994) Algunos factores ecológicos que determinan la distribución y abundancia del lobo marino Zalophus californianus, en el Golfo de California. Cienc Mar 20:535–553CrossRefGoogle Scholar
  10. Aurioles-Gamboa D, Sinsel F, Fox C, Alvarado E, Maravilla-Chávez O (1983) Winter migration of subadult male California sea lions Zalophus californianus in the southern part of Baja California. J Mammal 64:513–518. doi: https://doi.org/10.2307/1380369 CrossRefGoogle Scholar
  11. Aurioles-Gamboa D, Castillo S, Contreras AI, Barnes LG (2000) Patron latitudinal en caracteres dentarios del lobo marino de California en Norteamérica (Zalophus californianus californianus). In: XXV Reunión Internacional para el Estudio de los Mamíferos Marinos. La Paz, Baja California Sur, MéxicoGoogle Scholar
  12. Baker AR, Loughlin TR, Burkanov V, Matson CW, Trujillo RG, Calkins DG, Wickliffe JK, Bickham JW (2005) Variation of mitochondrial control region sequences of Steller sea lions: the three-stock hypothesis. J Mammal 86:1075–1084. doi: https://doi.org/10.1644/04-MAMM-A-113R1.1 CrossRefGoogle Scholar
  13. Bartholomew GA (1967) Seal and sea lion populations of the Channel Islands. In: Philbrick RN (ed) Proceedings of the symposium on the biology of the Calif. Islands, Santa Barbara Botanic Garden. Santa Barbara, CA, pp 229–243Google Scholar
  14. Beheregaray LB, Havill N, Gibbs J, Fritts T, Powell JR, Caccone G (2004) Giant tortoises are not so slow: rapid diversification and biogeographic consensus in the Galápagos. Proc Natl Acad Sci USA 101:6514–6519. doi: https://doi.org/10.1073/pnas.0400393101 CrossRefGoogle Scholar
  15. Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evol Int J Org Evol 57:1599–1609CrossRefGoogle Scholar
  16. Bickham JW, Patton JC, Loughlin TR (1996) High variability for control-region sequences in a marine mammal: implications for conservation and biogeography of Steller sea lion (Eumetopias jubatus). J Mammal 77:95–108. doi: https://doi.org/10.2307/1382712 CrossRefGoogle Scholar
  17. Boness DJ, Oftedal OT, Ono KA (1991) The effect of El Niño on pup development in the California Sea Lion (Zalophus californianus) I. Early postnatal growth. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 173–179CrossRefGoogle Scholar
  18. Bowen L, Aldridge BM, DeLong R, Melin S, Godínez C, Zavala A, Gulland F, Lowenstine L, Stott JL, Johnson ML (2006) MHC gene configuration variation in geographically disparate populations of California sea lions (Zalophus californianus). Mol Ecol 15:529–533. doi: https://doi.org/10.1111/j.1365-294X.2005.02612.x CrossRefGoogle Scholar
  19. Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 11:289–303CrossRefGoogle Scholar
  20. Browne RA, Anderson DJ, Houser JN, Cruz F, Glasgow KJ, Hodges CN, Massey G (1997) Genetic diversity and divergence of endangered Galápagos and Hawaiian petrel populations. Condor 99:812–815. doi: https://doi.org/10.2307/1370494 CrossRefGoogle Scholar
  21. Brunner S (2004) Fur seals and sea lions (Otariidae): identification of species and taxonomic review. Syst Biodivers 1:339–439. doi: https://doi.org/10.1017/S147720000300121X CrossRefGoogle Scholar
  22. Capella JJ, Flórez-González L, Falk-Fernández P, Palacios DM (2002) Regular appearance of otariid pinnipeds along the Colombian Pacific coast. Aquat Mamm 28:67–72Google Scholar
  23. Cenami Spada E, Hanggi EB, Schusterman RJ (1991) Variation in vocalizations and individual recognition in two subspecies of California sea lions. In: Abstracts of the 9th Biennial conference on the biology of marine mammals. Chicago, IllinoisGoogle Scholar
  24. Christie DM, Duncan RA, McBirney AR, Richards MA, White WM, Harp KS, Fox CG (1992) Drowned islands downstream from the Galapagos hotspot imply extended speciation times. Nature 355:246–248. doi: https://doi.org/10.1038/355246a0 CrossRefGoogle Scholar
  25. Clark PU, Archer D, Pollard D, Blum JD, Rial JA, Brovkin V, Mix AC, Pisias NG, Roy M (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quat Sci Rev 25:3,150–153,184, doi: https://doi.org/10.1016/j.quascirev.2006.07.008 CrossRefGoogle Scholar
  26. Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969PubMedPubMedCentralGoogle Scholar
  27. Davies JL (1958) The Pinnipedia: an essay in zoogeography. Geogr Rev 48:474–493. doi: https://doi.org/10.2307/211670 CrossRefGoogle Scholar
  28. Del Toro L, Heckel G, Camacho-Ibar VF, Schramm Y (2006) California sea lion (Zalophus californianus californianus) have lower chlorinated hydrocarbon contents in Baja California, México than in Southern California, USA. Environ Pollut 142:83–92. doi: https://doi.org/10.1016/j.envpol.2005.09.019 CrossRefGoogle Scholar
  29. DeLong RL, Antonelis GA, Oliver CW, Stewart BS, Lowry MC, Yochem PK (1991) Effects of the 1982–83 El Niño on several population parameters and diet of California Sea Lions on the California Channel Islands. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 166–172CrossRefGoogle Scholar
  30. Deméré TA, Berta A, Adam PJ (2003) Pinnipedimorph evolutionary biogeography. Bull Am Mus Nat Hist 279:32–76. doi: https://doi.org/10.1206/0003-0090(2003)279<0032:C>2.0.CO;2 CrossRefGoogle Scholar
  31. Dickerson BR, Ream RR, Vignieri SN, Bentzen P, Antonelis GA (2008) Population Structure as Revealed by mtDNA and Microsatellites in Northern Fur Seals, Callorhinus ursinus. In: Alaska Marine Science Symposium, Anchorage, AKGoogle Scholar
  32. Eibl-Eibesfeldt I (1984) The Galapagos seals. Part 1. Natural history of the Galapagos sea lion (Zalophus californianus wollebaeki, Siverstsen). In: Perry R (ed) Key environments: Galapagos. Pergamon Press, Oxford, pp 207–214Google Scholar
  33. Elorriaga-Verplancken F, Aurioles-Gamboa D (2008) Trace metal concentrations in the hair of Zalophus californianus pups and their relation to feeding habits. Biol Trace Elem Res 126:148–164. doi: https://doi.org/10.1007/s12011-008-8186-8 CrossRefGoogle Scholar
  34. Espinosa de los Reyes MG (2007) Variabilidad espacial de la dieta del lobo marino de California (Zalophus californianus californianus, Lesson 1828). MSc thesis, CICESE, Ensenada, BC, MéxicoGoogle Scholar
  35. Espinosa-Carreón TL, Strub PT, Beier E, Ocampo-Torres F, Glaxiola-Castro G (2004) Seasonal and interannual variability of satellite-derived chlorophyll pigment, surface height, and temperature off Baja California. J Geophys Res 109(C03039). doi: https://doi.org/10.1029/2003JC002105
  36. Excoffier L, Smouse P (1994) Using allele frequencies and geographic subdivision to reconstruct gene genealogies within a species. Molecular variance parsimony. Genetics 136:343–359PubMedPubMedCentralGoogle Scholar
  37. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  38. Francis JM, Heath CB (1991) Population abundance, pup mortality, and copulation frequency in the California sea lion in relation to the 1983 El Niño on San Nicolas Island. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 119–128CrossRefGoogle Scholar
  39. Friesen VL, Anderson DJ, Steeves TE, Jones H, Schreiber EA (2002) Molecular support for species status of the Nazca booby (Sula granti). Auk 119(3):820–826. doi: https://doi.org/10.1642/0004-8038(2002)119[0820:MSFSSO]2.0.CO;2 CrossRefGoogle Scholar
  40. Gallo-Reynoso JP, Solórzano-Velasco JL (1991) Two new sightings of California sea lions on the southern coast of México. Mar Mamm Sci 7:96. doi: https://doi.org/10.1111/j.1748-7692.1991.tb00557.x CrossRefGoogle Scholar
  41. García-Rodríguez FJ, Aurioles-Gamboa D (2004) Spatial and temporal variation in the diet of the California sea lion (Zalophus californianus) in the Gulf of California, México. Fish Bull (Washington, DC) 102:47–62Google Scholar
  42. Geist D (1996) On the emergence and submergence of the Galápagos Islands. Not Galap 56:5–9Google Scholar
  43. González-Suárez M, McCluney K, Aurioles-Gamboa D, Gerber LR (2006) Incorporating uncertainty in spatial structure for viability predictions: a case study of California sea lions. Anim Conserv 9:219–227. doi: https://doi.org/10.1111/j.1469-1795.2006.00022.x CrossRefGoogle Scholar
  44. Grehan J (2001) Biogeography and evolution of the Galapagos: integration of the biological and geological evidence. Biol J Linn Soc Lond 74(3):267–287. doi: https://doi.org/10.1006/bijl.2001.0576 CrossRefGoogle Scholar
  45. Guo S, Thomson E (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372. doi: https://doi.org/10.2307/2532296 CrossRefGoogle Scholar
  46. Harlin-Cognato A, Bickham JW, Loughlin TR, Honeycutt RL (2006) Glacial refugia and the phylogeography of Steller’s sea lion (Eumetopias jubatus) in the North Pacific. J Evol Biol 19:955–969. doi: https://doi.org/10.1111/j.1420-9101.2005.01052.x CrossRefGoogle Scholar
  47. Heath CB (2002) California, Galapagos, and Japanese Sea Lions. In: Perrin WF, Würsig B, Thewissen JGM (eds) Enciclopedia of Marine Mammals. Academic Press, San Diego, pp 180–186Google Scholar
  48. Hernández-Camacho C, Aurioles-Gamboa D, Laake J, Gerber L (2008a) Survival rates of the California sea lion, Zalophus californianus, in México. J Mammal 89:1059–1066. doi: https://doi.org/10.1644/07-MAMM-A-404.1 CrossRefGoogle Scholar
  49. Hernández-Camacho C, Aurioles-Gamboa D, Gerber L (2008b) Age-specific birth rates of California sea lions (Zalophus californianus) in the Gulf of California, México. Mar Mamm Sci 24:664–676. doi: https://doi.org/10.1111/j.1748-7692.2008.00199.x CrossRefGoogle Scholar
  50. Hey J (1991) The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics 128:831–840PubMedPubMedCentralGoogle Scholar
  51. Hickey BM (1998) Coastal oceanography of western North America from the tip of Baja California to Vancouver Island, coastal segment (8,E). In: Robinson AR, Brink KH (eds) The sea, vol 11, pp 345–393. Wiley, New York, pp 345–393Google Scholar
  52. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568. doi: https://doi.org/10.1093/molbev/msi145 CrossRefGoogle Scholar
  53. Jacobs DK, Haney TA, Louie KD (2004) Genes, diversity, and geologic process on the Pacific coast. Annu Rev Earth Planet Sci 32:601–652. doi: https://doi.org/10.1146/annurev.earth.32.092203.122436 CrossRefGoogle Scholar
  54. Kahru M, Marinone SG, Lluch-Cota SE, Parés-Sierra A, Mitchell BG (2004) Ocean-color variability in the Gulf of California: scales from days to ENSO. Deep Sea Res Part II Top Stud Oceanogr 51:139–146. doi: https://doi.org/10.1016/j.dsr2.2003.04.001 CrossRefGoogle Scholar
  55. Kannan K, Kajiwara N, Le Boeuf BJ, Tanabe S (2004) Organochlorine pesticides and polychlorinated biphenyls in California sea lions. Environ Pollut 131:425–434. doi: https://doi.org/10.1016/j.envpol.2004.03.004 CrossRefGoogle Scholar
  56. King JE (1983) Seals of the World. National History British Museum. Cornell University Press, New YorkGoogle Scholar
  57. Kooyman GL, Trillmich F (1986) Diving behavior of Galapagos sea lions. In: Gentry RL, Kooyman GL (eds) Fur seals—maternal strategies on land and at sea. Princeton University Press, Princeton, pp 209–220Google Scholar
  58. Koutavas A, Sachs JP (2008) Northern timing of deglaciation in the eastern equatorial Pacific from alkenone paleothermometry. Paleoceanography 23:PA4205. doi: https://doi.org/10.1029/2008PA001593 CrossRefGoogle Scholar
  59. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) Mega, version 2.1. Molecular Evolutionary Genetics Analysis software. Arizona State University, TempeGoogle Scholar
  60. Labrada MV, Aurioles-Gamboa D, Castro-González MI (2007) Relation of dental wear to the concentrations of essential minerals in teeth of the California sea lion Zalophus californianus californianus. Biol Trace Elem Res 114:107–126CrossRefGoogle Scholar
  61. Lawrence KT, Liu Z, Herbert TD (2006) Evolution of the eastern tropical Pacific through Plio-Pleistocene glaciation. Science 321:79–83. doi: https://doi.org/10.1126/science.1120395 CrossRefGoogle Scholar
  62. Le Boeuf BJ, Aurioles-Gamboa D, Condit R, Fox C, Gisiner R, Romero R, Sincel F (1983) Size and distribution of the California sea lion in México. Proc Calif Acad Sci 43:77–85Google Scholar
  63. Lea DW, Pak DK, Belanger CL, Spero HJ, Hall MA, Shackleton NJ (2006) Paleoclimate history of Galápagos surface waters over the last 135,000 yr. Quat Sci Rev 25:1152–1167. doi: https://doi.org/10.1016/j.quascirev.2005.11.010 CrossRefGoogle Scholar
  64. Lesson RP (1828) Phoque. In: Bory de Sanint-Vicent JBGM (ed) Dictionaire Classique d’Histoire Naturelle. Paris Rey et Gravier, ParisGoogle Scholar
  65. Lluch-Belda D (1969) El lobo marino de California, Zalophus californianus (Lesson, 1828). Allen 1880; observaciones sobre su ecología y explotación. Instituto Mexicano de Recursos Naturales Renovables, MéxicoGoogle Scholar
  66. Lowry MS, Maravilla-Chávez MO (2002) Abundancia de lobos marinos de California (Zalophus californianus) en Baja California, México y Estados Unidos de America durante julio y agosto del 2000. In: XXVII Reunión Internacional para el estudios de los Mamíferos Marinos. Veracruz, Ver. MéxicoGoogle Scholar
  67. Lowry MS, Boveng P, DeLong RJ, Oliver CW, Stewart BS, De Anda-Delgado H, Barlow J (1992) Status of the California sea lion (Zalophus californianus californianus) population in 1992. NOAA-TM-NMFS-SWFSC-LJ-92–32, La Jolla, pp 1–24Google Scholar
  68. Maldonado JE, Orta-Dávila F, Stewart BS, Geffen E, Wayne RK (1995) Intraspecific genetic differentiation in California sea lions (Zalophus californianus) from Southern California and the Gulf of California. Mar Mamm Sci 11:46–58. doi: https://doi.org/10.1111/j.1748-7692.1995.tb00273.x CrossRefGoogle Scholar
  69. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197. doi: https://doi.org/10.1016/S0169-5347(03)00008-9 CrossRefGoogle Scholar
  70. Maniscalco JM, Wynne K, Pitcher KW, Hanson MB, Melin SR, Atkinson S (2004) The occurrence of California sea lions in Alaska. Aquat Mamm 30:427–433. doi: https://doi.org/10.1578/AM.30.3.2004.427 CrossRefGoogle Scholar
  71. Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Am J Hum Biol 76:173–190. doi: https://doi.org/10.1353/hub.2004.0034 CrossRefGoogle Scholar
  72. Melin SR, DeLong RL (1999) At-sea distribution and diving behavior of California sea lion females from San Miguel Island, California. In: Browne DR, Mitchell KL, Chaney HW (eds) Proceeding of the fifth California islands symposium. Santa Barbara Museum of Natural History, Santa Barbara, pp 402–407Google Scholar
  73. Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375. doi: https://doi.org/10.1016/0169-5347(94)90057-4 CrossRefGoogle Scholar
  74. Morris PA, Oliver GW, Elliott J, Melin SR, DeLong RL (1999) El Niño 1998 and changes in California sea lion, Zalophus californianus, use of Año Nuevo island. In: Abstracts of the 13th Biennial Conference on the Biology of Marine Mammals, Wailea, HawaiiGoogle Scholar
  75. Newsome SD, Etnier MA, Koch PL, Aurioles-Gamboa D (2006) Using Carbon and Nitrogen isotopes to investigate reproductive strategies in Northeast Pacific otariids. Mar Mamm Sci 22:556–572. doi: https://doi.org/10.1111/j.1748-7692.2006.00043.x CrossRefGoogle Scholar
  76. Palacios DM, Félix F, Flórez-González L, Capella JJ, Chiluiza D, Haase BJM (1997) Sightings of Galápagos sea lions (Zalophus californianus wollebaeki) on the coasts of Colombia and Ecuador. Mammalia 61:114–116Google Scholar
  77. Peterson RS, Bartholomew GA (1967) The natural history and behavior of the California sea lion. Special publication no. 1. The American society of mammalogists, pp 1–79Google Scholar
  78. Porras-Peters H, Aurioles-Gamboa D, Cruz-Escalona VH, Koch PL (2008) Position, breadth and trophic overlap of sea lions (Zalophus californianus) in the Gulf of California, México. Mar Mamm Sci 24:554–576. doi: https://doi.org/10.1111/j.1748-7692.2008.00197.x CrossRefGoogle Scholar
  79. Rassmann K (1997) Evolutionary age of the Galapagos iguanas predates the age of the present Galapagos Islands. Mol Phylogenet Evol 7:158–172. doi: https://doi.org/10.1006/mpev.1996.0386 CrossRefGoogle Scholar
  80. Repenning CA, Ray CE, Grigourescou D (1979) Pinniped biogeography. In: Gray J, Boucot AJ (eds) Historical biogeography, plate tectonics, and the changing environment. Proceedings of the 37th Annual Biology Colloquium, and selected papers. Oregon State University, Corvallis, Oregon, pp 357-369Google Scholar
  81. Riedman M (1990) The Pinnipeds. Seals, sea lions, and walruses. University of California Press, Berkeley/Los AngelesGoogle Scholar
  82. Salazar S (2002) Lobo Marino y Lobo Peletero. In: Danulat E, Edgar GJ (eds) Reserva Marina de Galápagos. Linea Base de la biodiversidad. Fund Charles Darwin/Ser Par Nac Galap, Santa Cruz, Galápagos, Ecuador, pp 267–290Google Scholar
  83. Salazar S, Bustamante RH (2003) Effects of the 1997–98 El Niño on population size and diet of the Galápagos sea lion (Zalophus wollebaeki). Not Galap 62:40–45Google Scholar
  84. Salazar S, Michuy V (2008) Estado poblacional y conservación de los pinnípedos de las islas Galápagos. XIII Reunión de Trabajo de Especialístas en Mamíferos Acuáticos de América del Sur y 7˚ Congreso SOLAMAC. Montevideo, Uruguay, p 196Google Scholar
  85. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  86. Santamaría del Ángel E, Millán-Nuñez R, González-Silvera A, Müller-Karger F (2002) The color signature of the Ensenada Front and its seasonal and interannual variability. CCOFI Rep 43:155–161Google Scholar
  87. Schneider S, Roessli D, Excoffier L (2001) Arlequin, version 2. A software for population genetic data analysis. Genetic and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  88. Sivertsen E (1953) A new species of sea lion, Zalophus wollebaeki from the Galapagos Islands. Det Kong Nor Videnskaps Selsk Forh 26:1–3Google Scholar
  89. Sivertsen E (1954) A survey of the eared seals (family Otariidae) with remarks on the Antarctic seals collected by M/K “Norwegian” in 1928–1929. Det Nor Videnskaps—Akad OsloGoogle Scholar
  90. Stewart DT, Baker AJ (1994) Patterns of sequence variation in the mitochondrial D-loop region of shrews. Mol Biol Evol 11:9–21PubMedGoogle Scholar
  91. Szteren D (2006) Regionalización ecológica de las colonias reproductivas de Zalophus c. californianus en el Golfo de California, México. PhD thesis, CICIMAR-IPN, La Paz, BCS MéxicoGoogle Scholar
  92. Szteren D, Aurioles D, Gerber LR (2006) Population status and trends of the California sea lion (Zalophus californianus californianus) in the Gulf of California, México. In: Trites AW, Atkinson SK, DeMaster DP, Fritz LW, Gelatt TS, Rea LD, Wynne KM (eds) Sea Lions of the World. Alaska Sea Grant College Program, Lowell Wakefield Fisheries Symposium Series, Rhode Island, pp 369–384Google Scholar
  93. Trillmich F, Dellinger T (1991) The effects of El Niño on Galapagos Pinnipeds. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: Responses to environmental stress. Ecological Studies 88. Springer, New York, pp 66–74CrossRefGoogle Scholar
  94. Trillmich F, Limberger D (1985) Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67:19–22. doi: https://doi.org/10.1007/BF00378445 CrossRefGoogle Scholar
  95. Villegas-Amtmann S, Costa DP, 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 363:209–299. doi: https://doi.org/10.3354/meps07457 CrossRefGoogle Scholar
  96. Walker PL, Craig S (1979) Archaeological evidence concerning the prehistoric occurrence of sea mammals at Point Bennet, San Miguel Island. Calif Fish Game 65:50–54Google Scholar
  97. Walker PL, Kennett DJ, Jones TL, DeLong R (1999) Archaeological investigations at the Point Bennett pinniped rookery on San Miguel Island. In: Brown DR, Mitchell KC, Chaney HW (eds) Proceedings of the fifth California Islands symposium. US Department of the Interior Minerals Management Service, Pacific OCS Region, pp 628-632 Google Scholar
  98. Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). J Hered 95:144–153. doi: https://doi.org/10.1093/jhered/esh018 CrossRefGoogle Scholar
  99. Werner R, Hoernle K, van den Bogaard P, Ranero C, von Huene R, Korich D (1999) Drowned 14-m.y.-old Galápagos Archipelago off the coast of Costa Rica: Implications for tectonic and evolutionary models. Geology 27:499–502. doi:0.1130/0091-7613(1999)027<0499:DMYOGP>2.3.CO;2CrossRefGoogle Scholar
  100. Wolf JBW, Tautz D, Trillmich F (2007) Galápagos and California sea lions are separate species: genetic analysis of the genus Zalophus and its implications for conservation management. Front Zool 4:20. doi: https://doi.org/10.1186/1742-9994-4-20 CrossRefGoogle Scholar
  101. 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: https://doi.org/10.1186/1471-2148-8-150 CrossRefGoogle Scholar
  102. Wynen LP, Goldsworthy SD, Insley SJ, Adams M, Bickham JW, Francis J, Gallo-Reynoso JP, Hoelzel AR, Majluf P, White RWG, Slade R (2001) Phylogenetic relationships within the eared seals (Otariidae: Carnivora): Implications for the historical biogeography of the Family. Mol Phylogenet Evol 21:270–284. doi: https://doi.org/10.1006/mpev.2001.1012 CrossRefGoogle Scholar
  103. Zavala-González A, Mellink E (2000) Historical exploitation of the California sea lion, Zalophus californianus, in México. Mar Fish Rev 62:35–40Google Scholar
  104. Zavaleta-Lizárraga L (2003) Variaciones geográficas en morfometría craneal en machos adultos de lobo marino de California (Zalophus californianus) en México. MSc thesis, CICIMAR-IPN, MéxicoGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Yolanda Schramm
    • 1
  • S. L. Mesnick
    • 2
  • J. de la Rosa
    • 1
  • D. M. Palacios
    • 3
    • 4
  • M. S. Lowry
    • 2
  • D. Aurioles-Gamboa
    • 5
  • H. M. Snell
    • 6
    • 7
  • S. Escorza-Treviño
    • 8
  1. 1.Facultad de Ciencias MarinasUniversidad Autónoma de Baja CaliforniaEnsenadaMexico
  2. 2.Protected Resources Division, Southwest Fisheries Science CenterNOAA FisheriesLa JollaUSA
  3. 3.Joint Institute for Marine and Atmospheric ResearchUniversity of HawaiiHonoluluUSA
  4. 4.Environmental Research Division, Southwest Fisheries Science CenterNOAA FisheriesPacific GroveUSA
  5. 5.Centro Interdisciplinario de Ciencias MarinasInstituto Politécnico Nacional. Ave. IPN s/nLa PazMexico
  6. 6.Charles Darwin Research StationCharles Darwin FoundationGalápagosEcuador
  7. 7.Museum of Southwestern Biology, Department of BiologyUniversity of New MéxicoAlbuquerqueUSA
  8. 8.Department of Biological SciencesCalifornia State University Los AngelesLos AngelesUSA

Personalised recommendations