Marine Biology

, Volume 160, Issue 3, pp 641–652 | Cite as

δ15N and δ13C values in dental collagen as a proxy for age- and sex-related variation in foraging strategies of California sea lions

  • Fernando Elorriaga-VerplanckenEmail author
  • David Aurioles-Gamboa
  • Seth D. Newsome
  • Sergio F. Martínez-Díaz
Original Paper


We assessed the foraging habits of California sea lions, Zalophus californianus, from Isla Santa Margarita, BCS, Mexico, by analyzing δ13C and δ15N values of dentin collagen. Since dentin is deposited annually in growth layer groups (GLGs), it can be subsampled to construct ontogenetic isotopic profiles at the individual level. We drilled 20 canine teeth and obtained 141 samples for isotopic analysis that were assigned to age-specific categories from GLG-based estimated ages. Pups’ GLGs had the highest mean δ15N values and the lowest mean δ13C values, a pattern likely driven by the consumption of milk. Juveniles had δ15N values between those of pups and adult females, which may reflect continued nursing into the second year or preferential consumption of coastal benthic versus pelagic prey. Significant differences were observed between the sexes of adults; adult females had lower mean δ13C and δ15N values than adult males. Higher isotope values in adult males relative to females may reflect a higher trophic position, but differences in foraging grounds cannot be excluded as a potential explanation because tracking data are not available at this time. Evidence of intra-specific foraging diversification may be related to a strategy to reduce competition within and among age and sex categories.


Subadult Male Significant Negative Trend Dentin Sample Dentin Collagen Tooth Dentin 
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.



We thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) and the PIFI Program from the Instituto Politécnico Nacional (IPN) for the scholarships provided to FE-V. Financial support was provided by projects SIP-20120061-IPN and SEP-CONACYT-2004-C01-46806. We also thank the Secretaría de Medio Ambiente y Recursos Naturales throughout the Dirección General de Vida Silvestre Mexico for providing permits for field research D00.-700.-(2)01104 and D00.-700(2).-1917 and SGPA/DGVS.-0575.


  1. Altabet MA, Pilskaln C, Thunell R, Pride C, Sigman D, Chávez F, Francois R (1999) The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep-Sea Res 46:655–679Google Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson MJ (2004) PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  5. Aurioles-Gamboa D, Sinsel F, Fox C, Alvarado E, Maravilla O (1983) Winter migration of subadult male California sea lions (Zalophus californianus) in the southern part of Baja California. J Mammal 64:513–518CrossRefGoogle Scholar
  6. Aurioles-Gamboa D, Koch PL, Le Bœuf BJ (2006) Differences in foraging ecology of Mexican and California elephant seals: evidence from stable isotopes in pups. Mar Mammal Sci 22:1–13CrossRefGoogle Scholar
  7. Aurioles-Gamboa D, Newsome SD, Salazar-Pico S, Koch PL (2009) Stable isotope differences between sea lions (Zalophus) from the Gulf of California and Galapagos Islands. J Mammal 90:1410–1420CrossRefGoogle Scholar
  8. Bartholomew GA, Boolootian RA (1960) Numbers and population structure of the pinnipeds of the Channel Islands. J Mamm 41:366–375CrossRefGoogle Scholar
  9. Bautista VA (2002) Alimentación del lobo marino de California (Zalophus californianus californianus, Lesson 1828) y su relación con los pelágicos menores en Bahía Magdalena, B.C.S., México. Dissertation, Universidad Nacional Autónoma de México (UNAM)Google Scholar
  10. Boness DJ, Bowen WD (1996) Evolution of maternal care in pinnipeds. Biosci 46:645–654CrossRefGoogle Scholar
  11. Burton RK, Koch PL (1999) Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585CrossRefGoogle Scholar
  12. Camalich-Carpizo J (2011) Registro de la variabilidad oceanográfica en peces demersales y depredadores tope de la zona oceánica frontal de Bahía Magdalena. Dissertation, CICIMAR-IPN, La Paz BCS, MéxicoGoogle Scholar
  13. Carretta JV, Forney KA, Muto MM, Barlow J, Baker J, Hanson B, Lowry MS (2007) US Pacific marine mammal stock assessments: 2006. Technical memorandum NOAA-TM-NMFS-SWSCGoogle Scholar
  14. Clutton-Brock TH, Iason GR, Guinness FE (1987) Sexual segregation and density-related changes in habitat use in male and female deer (Cervus elaphus). J Zool Lond 211:275–289CrossRefGoogle Scholar
  15. Da Silva J, Neilson JD (1985) Limitations of using otholits recovered in scats to estimate prey consumption in seals. Can J Fish Aquat Sci 42:1439–1442CrossRefGoogle Scholar
  16. Dellinger T, Trillmich F (1988) Estimating diet composition from scat analysis in otariid seals (Otariidae): is it reliable? Can J Zool 66:1865–1870CrossRefGoogle Scholar
  17. DeNiro MJ, Epstein S (1978) Influence of the diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Ac 42:495–506CrossRefGoogle Scholar
  18. Eberhardt LL, Sinnif DB (1977) Population dynamics and marine mammal management policies. J Fish Res Board Can 34:183–190CrossRefGoogle Scholar
  19. Elorriaga-Verplancken F (2009) Variación de δ15N y δ13C en colágeno dental de lobos marinos del género Zalophus: patrones ontogénicos y geográficos. Dissertation, CICIMAR-IPN, La Paz BCS, MéxicoGoogle Scholar
  20. Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155CrossRefGoogle Scholar
  21. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: Foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  22. Fry B, Wainright SC (1991) Diatom sources of 13C-rich carbon in marine food webs. Mar Ecol Prog Ser 76:149–157CrossRefGoogle Scholar
  23. García-Aguilar M, Aurioles-Gamboa D (2003) Cuidado materno en el lobo marino de California (Zalophus californianus) de Los Islotes, Golfo de California, México. Cienc Mar 29:573–583Google Scholar
  24. 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, Mexico. Fish Bull 102:47–62Google Scholar
  25. Gautier-Hion A (1980) Seasonal variations of diet related to species and sex in a community of Cercopithecus monkeys. J Anim Ecol 49:237–269CrossRefGoogle Scholar
  26. Goericke R, Fry B (1994) Variations of marine δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Global Biogeochem Cy 8:85–90CrossRefGoogle Scholar
  27. Graham B, Koch PL, Newsome SD, McMahon K, Aurioles-Gamboa D (2010) Using isoscapes to trace the movement and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE (eds) Isoscapes: understanding movement, pattern, and process on earth through isotope mapping, 1st edn. Springer, Berlin, pp 299–318Google Scholar
  28. Hobson KA, Sease JL (1998) Stable isotope analysis of tooth annuli reveals temporal dietary records: an example using Steller Sea lions. Mar Mammal Sci 14:116–129CrossRefGoogle Scholar
  29. Hobson KA, Sease JL, Merrick RL, Piatt JF (1997) Investigating trophic relationships of pinnipeds in Alaska and Washington using stable isotope ratios of nitrogen and carbon. Mar Mammal Sci 13:114–132CrossRefGoogle Scholar
  30. Jenkins SG, Partridge ST, Stephenson TR, Farley SD, Robbins CT (2001) Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia 129:336–341Google Scholar
  31. Klevezal GA (1996) Recording structures of mammals: determination of age and reconstruction of life history. A. A. Balkema, RotterdamGoogle Scholar
  32. Koch PL (2007) Isotopic study of the biology of modern and fossil vertebrates. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Scientific Publications, Boston, pp 99–154CrossRefGoogle Scholar
  33. Kuhn CE, Aurioles-Gamboa D, Weise MJ, Costa DP (2006) Oxygen stores of California sea lion pups: implications for diving ability. Sea Lions of the World. Alaska Sea Grant College Program. AK-SG-06-01Google Scholar
  34. Kurle CM, Worthy GAJ (2001) Stable isotope assessment of temporal and geographic differences in feeding ecology of Northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126:254–265CrossRefGoogle Scholar
  35. Kurle CM, Worthy GAJ (2002) Stable nitrogen and carbon isotopes ratios in multiple tissues of the Northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Mar Ecol Prog Ser 236:289–300CrossRefGoogle Scholar
  36. Laws EA, Popp BN, Bidigare RR, Kennicutt MC, Macko DS (1995) Dependence of phytoplankton carbon isotopic composition on growth rate and (CO2)aq: theoretical considerations and experimental results. Geochim Cosmochim Ac 59:1131–1138CrossRefGoogle Scholar
  37. Le Boeuf BJ, Crocker DE, Blackwell SB, Morris PA, Thorson PH (1993) Sex differences in foraging in Northern elephant seals. In: Boyd L (ed) Marine mammals: advances in behavioral and population biology. Oxford University Press, UK, pp 149–178Google Scholar
  38. Lewis R, O’ Connell TC, Lewis M, Campagna C, Hoelzel AR (2006) Sex-specific foraging strategies and resource partitioning in the southern elephant seal (Mirounga leonina). Proc R Soc 273:2901–2907CrossRefGoogle Scholar
  39. Lowry MS, Maravilla O (2005) Proceedings of the sixth California islands symposium, Ventura, California, December 1–3, 2003. National Park Service Technical Publication CHIS-05-01, Institute for Wildlife Studies, Arcata, CAGoogle Scholar
  40. Macko SA, Estep MLF (1984) Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Org Geochem 6:787–790CrossRefGoogle Scholar
  41. Martínez del Río C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  42. Mate BR (1975) Annual migrations of the sea lions Eumetopias jubatus and Zalophus californianus along the Oregon coast. Rapp PV Réun Cons Int Explor Mer 169:455–461Google Scholar
  43. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  44. Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Scientific Publications, Boston, pp 138–157Google Scholar
  45. Minagawa M, Wada E (1984) Stepwise δ15N enrichment along food chains. Further evidence and the relation between δ15N and animal age. Geochim Cosmochim Ac 48:1135–1140CrossRefGoogle Scholar
  46. Newsome SD, Koch PL, Etnier MA, Aurioles-Gamboa D (2006) Using carbon and nitrogen isotope values to investigate maternal strategies in Northeast Pacific Otariids. Mar Mammal Sci 22:1–18CrossRefGoogle Scholar
  47. Newsome SD, Etnier MA, Monson DH, Fogel ML (2009) Retrospective characterization of ontogenetic shifts in killer whale diets via δ13C and δ15N analysis of sectioned teeth. Mar Ecol Prog Ser 374:229–242CrossRefGoogle Scholar
  48. Newsome SD, Clementz M, Koch PL (2010) Using stable isotope biochemistry to study marine mammal ecology. Mar Mammal Sci 26:509–572Google Scholar
  49. Odell DK (1975) Breeding biology of the California sea lion, Zalophus californianus. Rapp PV Réun Cons Int Explor Mer 169:374–378Google Scholar
  50. Orr AJ, Harvey JT (2001) Quantifying errors associated with using fecal samples to determine the diet of the California sea lion (Zalophus californianus). Can J Zool 79:1080–1087Google Scholar
  51. Orr RT, Schonewald J, Kenyon KW (1970) The California sea lion: Skull growth and comparison of two populations. Proc Calif Acad Sci 37:381–394Google Scholar
  52. Owens PJN (1987) Natural variations in δ15N in the marine environment. Adv Mar Biol 24:389–451CrossRefGoogle Scholar
  53. Páez-Rosas D, Aurioles-Gamboa D (2010) Alimentary Niche partitioning in the Galapagos sea lion, Zalophus wollebaeki. Mar Biol 157:2769–2781CrossRefGoogle Scholar
  54. Peterson RS, Bartholomew GA (1967) The natural history and behavior of the California sea lion. Am Soc Mammal Special Publ 1:79Google Scholar
  55. Pilson EEQ, Kelly AL (1962) Comparison of the milk from Zalophus californianus, the California sea lion. Science 135:104–105CrossRefGoogle Scholar
  56. Post D (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  57. Riofrío-Lazo M, Aurioles-Gamboa D, Le Boeuf BJ (2012) Ontogenetic changes in feeding habits of northern elephant seals revealed by δ15N and δ13C analysis of growth layers in teeth. Mar Ecol Prog Ser 450:229–241CrossRefGoogle Scholar
  58. Scheffer VB (1950) Growth layers on the teeth of Pinnipedia as an indication of age. Science 112:309–311CrossRefGoogle Scholar
  59. Sinisalo T, Jones RI, Helle E, Valtonen ET (2008) Changes in diets of individual Baltic ringed seals (Phoca hispida botnica) during their breeding season inferred from stable isotope analysis of multiple tissues. Mar Mammal Sci 24:159–170CrossRefGoogle Scholar
  60. Szteren D, Aurioles-Gamboa D, Gerber L (2006) Population status and trends of the California Sea Lion (Zalophus californianus californianus) in the Gulf of California, Mexico. 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, University of Alaska Fairbanks, AK-SG-06-01, pp 369–384Google Scholar
  61. Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue–diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19:3239–3247CrossRefGoogle Scholar
  62. 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 363:299–309CrossRefGoogle Scholar
  63. Voss M, Dippner JW, Montoya JP (2001) Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical North Pacific Ocean. Deep Sea Res I 48:1905–1921CrossRefGoogle Scholar
  64. Wada E, Hattori A (1991) Nitrogen in the sea: forms, abundances and rate processes. CSC Press, Boca Raton, FLGoogle Scholar
  65. Walker J, Macko SA (1999) Dietary studies of marine mammals using stable carbon and nitrogen isotopic ratios of teeth. Mar Mammal Sci 15:314–334CrossRefGoogle Scholar
  66. Weise MJ, Costa DP (2007) Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. J Exp Biol 210:278–289CrossRefGoogle Scholar
  67. Wolf JB, Harrod C, Brunner S, Salazar S, Trillmich F, Tautz D (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galapagos sea lion populations. BMC Evol Biol 8:150CrossRefGoogle Scholar
  68. Young BG, Loseto LL, Ferguson SH (2010) Diet differences among age classes of Arctic seals: evidence from stable isotopes and mercury biomarkers. Polar Biol 33:153–162CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Fernando Elorriaga-Verplancken
    • 1
    Email author
  • David Aurioles-Gamboa
    • 1
  • Seth D. Newsome
    • 2
  • Sergio F. Martínez-Díaz
    • 3
  1. 1.Laboratorio de Ecología de Pinnípedos “Burney J. Le Boeuf”, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico NacionalLa Paz, Baja California SurMexico
  2. 2.Department of Zoology and PhysiologyUniversity of WyomingLaramieUSA
  3. 3.Departamento de Desarrollo de TecnologíasCentro Interdisciplinario de Ciencias Marinas, Instituto Politécnico NacionalLa Paz, Baja California SurMexico

Personalised recommendations