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Oecologia

, Volume 188, Issue 1, pp 263–275 | Cite as

Temporal records of diet diversity dynamics in individual adult female Steller sea lion (Eumetopias jubatus) vibrissae

  • A. C. Doll
  • B. D. Taras
  • C. A. Stricker
  • L. D. Rea
  • T. M. O’Hara
  • A. P. Cyr
  • S. McDermott
  • T. M. Loomis
  • B. S. Fadely
  • M. B. Wunder
Community ecology – original research

Abstract

Detailed information on the nutrition of free-ranging mammals contributes to the understanding of life history requirements, yet is often quite limited temporally for most species. Reliable dietary inferences can be made by analyzing the stable carbon (C) and nitrogen (N) isotopic values (δ13C and δ15N) of some consumer tissues; exactly which tissue is utilized dictates the inferential scope. Steller sea lion (SSL) vibrissae are grown continuously without shedding and thus provide a continuous multi-year record of dietary consumption. We applied a novel kernel density approach to compare the δ13C and δ15N values along the length of SSL vibrissae with δ13C and δ15N distributions of potential prey species. This resulted in time-series of proportion estimates of dietary consumption for individual SSL. Substantial overlap in δ13C and δ15N distributions for prey species prevented a discrete species-scale assessment of SSL diets; however, a post hoc correlational analysis of diet proportion estimates revealed grouping by trophic level. Our findings suggest that adult female SSL diets in the western and central Aleutian Islands shift significantly according to season: diets contain a higher proportion of lower trophic level species (Pacific Ocean perch, northern rockfish, Atka mackerel and walleye pollock) in the summer, whereas in the winter SSL consume a much more diverse diet which includes a greater proportion of higher trophic level species (arrowtooth flounder, Kamchatka flounder, darkfin sculpin, Pacific cod, Pacific octopus, rock sole, snailfish, and yellow Irish lord).

Keywords

Stable isotope Carbon Nitrogen Trophic Kernel density 

Notes

Acknowledgements

We would like to thank the field teams of the Alaska Department of Fish and Game (ADF&G) and the Marine Mammal Laboratory (MML) for collection of vibrissae from adult female Steller sea lions and the vessel crew of the R/V Norseman II for their support of this project. Analysis of stable isotopes in vibrissae was funded by NOAA through NA13NMF4720041 to ADF&G. We would like to thank Ocean Peace Inc. for their donation and shipment of fish samples to UAF, subsampled from their commercial fishery in the Aleutian Islands in 2013 and 2014. Prey stable isotope analysis was sponsored by the Cooperative Institute for Alaska Research with funds from the National Oceanic and Atmospheric Administration under cooperative agreement NA13OAR4320056 with the University of Alaska (LDR and TMO). Additional funding for analysis of prey was provided through an INBRE Undergraduate Summer Research Award to G. Johnson. We thank ADF&G for providing salary support and supplies for initial fish sampling, and the WTL for providing storage, sample processing facilities and equipment for chemical analyses. We thank E. Audette, M. Campbell, L. Correa, E. Decker, Z. Goeden, A. Grimes, J. Harley, G. Johnson, S. Kennedy and for assistance with subsampling tissues and the Alaska Stable Isotope Facility at UAF for analysis. We also thank A. Parnell for consultations regarding the adaptation of Bayesian SIMMs for time series diet modeling. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Steller sea lion vibrissae were collected under authority of MMPA permit #14326 and 18528 to MML and #14325 to ADF&G, and under ACUC protocols A-NW2010-4 and A-NW2013-2 to MML, 2010-14R to ADF&G, and 594759-2 to LDR. Collection of Atka mackerel and Pacific cod in NMFS Fisheries Management Area 543 was permitted under NOAA Letter of Acknowledgment (LOA): 2013-01.

Author contribution statement

LDR, CAS and MBW originally formulated the idea and developed methodology with ACD and BDT; LDR, BSF and TMO organized fieldwork and sample collection; ACD and BDT collaborated in data analysis model development, and ACD and BDT wrote the manuscript; all other authors provided editorial advice.

Supplementary material

442_2018_4173_MOESM1_ESM.pdf (2 mb)
Supplementary material 1 (PDF 2026 kb)

References

  1. Atkinson S, DeMaster DP, Calkins DG (2008) Anthropogenic causes of the western Steller sea lion Eumetopias jubatus population decline and their threat to recovery. Mamm Rev 38:1–18CrossRefGoogle Scholar
  2. Calhoun JB, Casby JU (1958) Calculation of home range and density of small mammals. US Department of Health, Education, and Welfare, Public Health Service. No. 55Google Scholar
  3. Cherel Y, Kernaléguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol Lett 5:830–832CrossRefPubMedPubMedCentralGoogle Scholar
  4. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197(4300):261–263.  https://doi.org/10.1126/science.327543 CrossRefPubMedGoogle Scholar
  5. Focken U, Becker K (1998) Metabolic fractionation of stable carbon isotopes: implications of different proximate compositions for studies of aquatic food webs using δ13C data. Oecologia 115:337–343CrossRefPubMedGoogle Scholar
  6. Fontugne MR, Duplessy JC (1981) Organic carbon isotopic fractionation by marine plankton in the temperature range −1 to 31 °C. Oceanol Acta 4(1):85–90Google Scholar
  7. Greaves DK, Hammill MO, Eddington JD, Pettipas D, Schreer JF (2004) Growth rate and shedding of vibrissae in the gray seal, Halichoerus grypus: a cautionary note for stable isotope data analysis. Mar Mamm Sci 20:296–304CrossRefGoogle Scholar
  8. Gunderson DR (1971) Reproductive patterns of Pacific ocean perch (Sebastodes alutus) off Washington and British Columbia and their relation to bathymetric distribution and seasonal abundance. J Fish Res Board Can 28:417–425CrossRefGoogle Scholar
  9. Hayfield T, Racine JS (2008) Nonparametric econometrics: the np package. J Stat Softw 27(5). http://www.jstatsoft.org/v27/i05/. Accessed 5 Aug 2015
  10. Hirons AC, Schell DM, St. Aubin DJ (2001) Growth rates of vibrissae of harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus). Can J Zool 79:1053–1061CrossRefGoogle Scholar
  11. Hobson KA (2007) Isotopic tracking of migrant wildlife. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Publishing, Malden, pp 155–175CrossRefGoogle Scholar
  12. 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 Mamm Sci 13(1):114–132CrossRefGoogle Scholar
  13. Hobson KA, Barnett-Johnson R, Cerling T (2010) Using isoscapes to track animal migration. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern and process on earth through isotope mapping. Springer, New York, pp 273–298CrossRefGoogle Scholar
  14. Hoffman JC, Sutton TT (2010) Lipid correction for carbon stable isotope analysis of deep-sea fishes. Deep Sea Res 57:956–964CrossRefGoogle Scholar
  15. Horne JS, Garton EO (2006) Likelihood cross-validation versus least squares-cross-validation for choosing the smoothing parameter in kernel home-range analysis. J Wildl Manag 70:641–648CrossRefGoogle Scholar
  16. Horton HF (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest)–Dover and rock soles. U.S. Fish Wildl Serv Biol Rep 82(1.123):1–17Google Scholar
  17. Jennrich RI, Turner FB (1969) Measurement of non-circular home range. J Theor Biol 22:227–237CrossRefPubMedGoogle Scholar
  18. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27CrossRefGoogle Scholar
  19. Kernaléguen L, Cazelles B, Arnould JPY, Richard P, Guinet C, Cherel Y (2012) Long-term species, sexual and individual variations in foraging strategies of fur seals revealed by stable isotopes in whiskers. PLoS One 7(3):e32916CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kernohan BJ, Gitzen RA, Millspaugh JJ (2001) Analysis of animal space use and movements. In: Milspaugh JJ, Marzluff JM (eds) Radio tracking and animal populations. Academic, New York, pp 125–166CrossRefGoogle Scholar
  21. Kurle CM, Sinclair EH, Edwards AE, Gudmundson CJ (2011) Temporal and spatial variation in the δ 15N and δ 13C values of fish and squid from Alaska waters. Mar Biol 158:2389–2404CrossRefGoogle Scholar
  22. Ling JK (1970) Pelage and molting in wild mammals with special reference to aquatic forms. Q Rev Biol 45(1):16–54CrossRefPubMedGoogle Scholar
  23. Logerwell EA, Aydin K, Barbeaux S, Brown E, Conners ME, Lowe S, Orr JW, Ortiz L, Reuter R, Spencer P (2005) Geographic patterns in the demersal ichthyofauna of the Aleutian Islands. Fish Oceanogr 14(SUPPL. 1):93–112CrossRefGoogle Scholar
  24. Lowe S, Ianelli J, Zenger H, Lauth R (2003) Stock assessment of Aleutian Islands Atka Mackerel. North Pacific Fishery Management Council Bering Sea/Aleutian Islands SAFE (Stock Assessment and Fishery Evaluation) ReportsGoogle Scholar
  25. Lowther AD, Goldsworthy SD (2011) Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) colonies using stable isotope analysis. Mar Mamm Sci 27(3):567–586CrossRefGoogle Scholar
  26. McCain BB, Miller SD, Wakefield WWII (2005) Life history, geographical distribution, and habitat associations of 82 west coast Groundfish species: a literature review. Appendix H in Pacific Coast Groundfish Fisheries Management Plan, Essential Fish Habitat Designation and Minimization of Adverse Impact, Draft Environmental Impact Statement, 97220 (December). http://www.westcoast.fisheries.noaa.gov/publications/nepa/groundfish/groundfish_efh_eis/fmp-appendix-b2.pdf. Accessed 20 Nov 2015
  27. National Marine Fisheries Service (2013) Status review of the eastern distinct population segment of Steller Sea Lion (Eumetopias jubatus). Protected Resources Division, Alaska Region, National Marine Fisheries Service, 709 West 9th St, Juneau, Alaska 99802Google Scholar
  28. National Marine Fisheries Service (NMFS) (2008) Recovery plan for the Steller sea lion (Eumetopias jubatus). Revision. National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Department of Commerce, Silver Spring, Maryland, USAGoogle Scholar
  29. Parnell AC, Phillips DL, Bearhop S, Jackson AL, Semmens BX, Ward EJ, Moore JW, Grey J, Kelly DJ, Inger RL (2013) Bayesian stable isotope mixing models. Environmetrics 24(6):387–399Google Scholar
  30. Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481CrossRefGoogle Scholar
  31. Pitcher KW, Olesiuk PF, Brown RF, Lowry MS, Jeffries SJ, Sease JL, Perryman WL, Stinchcomb CE, Lowry LF (2007) Abundance and distribution of the eastern North Pacific Steller sea lion (Eumetopias jubatus) population. Fish Bull 107:102–115Google Scholar
  32. Rea LD, Castellini JM, Correa L, Fadely BS, O’Hara TM (2013) Maternal Steller sea lion diets elevate fetal mercury concentrations in area of population decline. Sci Total Environ 454–455:277–282CrossRefPubMedGoogle Scholar
  33. Rea LD, Christ AM, Hayden AB, Stegall VK, Farley SD, Stricker CA, Mellish JE, Maniscalco JM, Waite JN, Burkanov V, Pitcher KW (2015) Age-specific vibrissae growth rates: a tool for determining the timing of ecologically important events in Steller sea lions. Mar Mamm Sci 31(3):1213–1233.  https://doi.org/10.1111/mms.12221 CrossRefGoogle Scholar
  34. Rea LD, Fadely BS, Farley SD, Avery JP, Dunlap-Harding WS, Stegall VK, Eischens CAB, Gelatt TS, Pitcher KW (2016) Comparing total body lipid content of young-of-the-year Steller sea lions among regions of contrasting population trends. Mar Mamm Sci 32(4):1200–1218.  https://doi.org/10.1111/mms.12327 CrossRefGoogle Scholar
  35. Rickey MH (1995) Maturity, spawning, and seasonal movement of arrowtooth flounder, Atheresthes stomis, off Washington. Fish Bull 93:127–138Google Scholar
  36. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 19 July 2015
  37. Scherer RD, Doll AC, Rea LD, Christ AM, Stricker CA, Witteveen B, Kline TC, Kurle CM, Wunder MB (2015) Isotope values in pup whiskers reveal geographic variation in diets of gestating Steller sea lions (Eumetopias jubatus). Mar Ecol Prog Ser 527:261–274CrossRefGoogle Scholar
  38. Sigler MF, Tollit DJ, Vollenweider J, Thedinga J, Csepp DJ, Womble JN, Wong MA, Rehberg MJ, Trites AW (2009) Steller sea lion foraging response to seasonal changes in prey availability. Mar Ecol Prog Ser 388:243–261CrossRefGoogle Scholar
  39. Sinclair EH, Zeppelin TK (2002) Seasonal and spatial differences in diet in the western stock of Steller sea lions (Eumetopias Jubatus). J Mamm 83(4):973–990CrossRefGoogle Scholar
  40. Stock BC, Semmens BX (2013) MixSIAR GUI User Manual, version 1.0. http://conserver.iugo-cafe.org/user/brice.semmens/MixSIAR. Accessed 10 Apr 2014
  41. Stricker CA, Christ AM, Wunder MB, Doll AC, Farley SD, Rea LD, Rosen DAS, Scherer RD, Tollit DJ (2015) Carbon and nitrogen isotope discrimination for Steller sea lion (Eumetopias jubatus) vibrissae relative to milk and fish/invertebrate diets. Mar Ecol Prog Ser 523:255–266CrossRefGoogle Scholar
  42. Trites AW, Calkins DG (2008) Diets of mature male and female Steller sea lions (Eumetopias jubatus) differ and cannot be used as proxies for each other. Aquat Mamm 34(1):25–34CrossRefGoogle Scholar
  43. Wainright SC, Fry B (1994) Seasonal variation of the stable isotopic compositions of coastal marine plankton from woods hole, Massachusetts and Georges Bank. Estuaries 17(3):552–560CrossRefGoogle Scholar
  44. Womble JN, Sigler MF (2006) Seasonal availability of abundant, energy-rich prey influences the abundance and diet of a marine predator, the Steller sea lion Eumetopias jubatus. Mar Ecol Prog Ser 325:281–293CrossRefGoogle Scholar
  45. Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168CrossRefGoogle Scholar
  46. Worton BJ (1995) Using Monte Carlo simulation to evaluate kernel-based home range estimators. J Wildl Manag 59:794–800CrossRefGoogle Scholar
  47. Yang MS (2003) Food habits of the important groundfishes of the Aleutian Islands in 1994 and 1997. AFSC Processed report 2003–07 (National Marine Fisheries Service)Google Scholar
  48. Yang MS, Nelson MW (2000) Food habits of the commercially important groundfishes in the Gulf of Alaska in 1990, 1993, and 1996. NOAA Tech. Memo. NMFS-AFSC-112 (U.S. Dep. Commer.)Google Scholar
  49. York AE, Merrick RL, Loughlin TR (1996) An analysis of the Steller sea lion metapopulation in Alaska. In: McCul-lough DR (ed) Metapopulation and wildlife conservation. Island Press, Washington, DC, pp 259–292Google Scholar
  50. Zeppelin TK, Tollit DJ, Call KA, Orchard TJ, Gudmundson CJ (2004) Sizes of walleye pollock (Theragra chalcogramma) and Atka mackerel (Pleurogrammus monopterygius) consumed by the western stock of Steller sea lions (Eumetopias jubatus) in Alaska from 1999 to 2000. Fish Bull 102(3):509–521Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • A. C. Doll
    • 1
  • B. D. Taras
    • 2
  • C. A. Stricker
    • 3
  • L. D. Rea
    • 2
    • 4
  • T. M. O’Hara
    • 5
  • A. P. Cyr
    • 6
  • S. McDermott
    • 7
  • T. M. Loomis
    • 8
  • B. S. Fadely
    • 9
  • M. B. Wunder
    • 1
  1. 1.Department of Integrative BiologyUniversity of Colorado-DenverDenverUSA
  2. 2.Alaska Department of Fish and Game, Division of Wildlife ConservationFairbanksUSA
  3. 3.US Geological Survey, Fort Collins Science CenterDenverUSA
  4. 4.Institute of Northern EngineeringUniversity of Alaska FairbanksFairbanksUSA
  5. 5.Department of Veterinary MedicineUniversity of Alaska FairbanksFairbanksUSA
  6. 6.College of Fisheries and Ocean SciencesUniversity of Alaska FairbanksFairbanksUSA
  7. 7.Alaska Fisheries Science CenterNational Marine Fisheries Service, NOAASeattleUSA
  8. 8.Ocean Peace IncAnchorageUSA
  9. 9.Marine Mammal Laboratory, Alaska Fisheries Science CenterNational Marine Fisheries Service, NOAASeattleUSA

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