, Volume 10, Issue 4, pp 376–393 | Cite as

Serum Chemistry Reference Ranges for Steller Sea Lion (Eumetopias jubatus) Pups from Alaska: Stock Differentiation and Comparisons Within a North Pacific Sentinel Species

  • Michelle E. LanderEmail author
  • Brian S. Fadely
  • Thomas S. Gelatt
  • Lorrie D. Rea
  • Thomas R. Loughlin
Original Contribution


Blood chemistry and hematologic reference ranges are useful for population health assessment and establishing a baseline for future comparisons in the event of ecosystem changes due to natural or anthropogenic factors. The objectives of this study were to determine if there was any population spatial structure for blood variables of Steller sea lion (Eumetopias jubatus), an established sentinel species, and to report reference ranges for appropriate populations using standardized analyses. In addition to comparing reference ranges between populations with contrasting abundance trends, data were examined for evidence of disease or nutritional stress. From 1998 to 2011, blood samples were collected from 1,231 pups captured on 37 rookeries across their Alaskan range. Reference ranges are reported separately for the western and eastern distinct population segments (DPS) of Steller sea lion after cluster analysis and discriminant function analysis (DFA) supported underlying stock structure. Variables with greater loading scores for the DFA (creatinine, total protein, calcium, albumin, cholesterol, and alkaline phosphatase) also were greater for sea lions from the endangered western DPS, supporting previous studies that indicated pup condition in the west was not compromised during the first month postpartum. Differences between population segments were likely a result of ecological, physiological, or age related differences.


blood bootstrap Eumetopias jubatus health status hematology nutritional stress reference ranges serum chemistry Steller sea lion 



We thank the entire staff of the Alaska Ecosystems Program at the National Marine Mammal Laboratory (NMML), including P. Brown, V. Burkanov, K. Call, B. Caruso, B. Dickerson, S. Finneseth, L. Fritz, C. Gudmundson, C. Kuhn, R. Ream, J. Sease, J. Sterling, W. Testa, J. Thomason, R. Towell, and T. Zeppelin for all of their assistance with capturing and handling sea lions and for sample collection and processing. We also thank all members of the ADF&G field collections team including A. Baylis, K. Beckmen, R. Braun, K. Burek, J. Crye, C. Eischens, D. Faquier, C. Flatten, T. Haase, M. Haulena, C. Jewett, S. Johnson, C. Kaplan, M. Lambert, J. King, M. Litzow, S. Moore, B. Murphy, G. O’Corry-Crowe, K. Pitcher, M. Rehberg, J. Richmond, E. Schoen, R. Small, G. Snedgen, G. Spencer, V. Stegall, C. Stinchcomb, W. Taylor, D. Tollit, J. Westlund, E. Wilson, K. White, and J. Womble. We further thank J. Baily, E. Boerner, A. Burdin, B. DeLong, F. Gulland, H. Harris, D. Hennen, R. Jenkinson, T. Hobbs, J. Mellish, Y. Miyake, P. Nicklen, S. Norman, J. Scordino, D. Thompson, S. Trumble, V. Vanek, L. Wheeler, B. Wright, and crews of the M/V TIGLAX, M/V PACIFIC STAR, M/V Morning Star, R/V NORSEMAN, R/V MEDEIA, and the AEP field camps for their field support. D. Johnson and H. Smith provided valuable assistance with data analysis, D. Greig (per L. Schwacke) provided some code and advice, and G. Duker, B. Dickerson, S. Norman, and two anonymous reviewers provided constructive comments on the manuscript. This work was supported by the NMML and by NOAA cooperative agreement funding to ADF&G. Sample collections were conducted under the authority of Federal MMPA/ESA Permits 782-1447, 782-1532, 782-1768, 782-1889, and 14326 issued to NMML and permits 358-1564 and 358-1769 issued to ADF&G. The findings and conclusions in the paper are those of the authors and do not necessarily represent the views of the NMFS, NOAA. Reference to trade names does not imply endorsement by the NMFS, NOAA.


  1. Bickham JW, Loughlin TR, Wickliffe JK, Burkanov VN (1998) Geographic variation in the mitochondrial DNA of Steller sea lions: haplotype diversity and endemism in the Kuril Islands. Biosphere Conservation 1:107-117.Google Scholar
  2. Bickham JW, Patton JC, Loughlin TR (1996) High variability for control-region sequences in a marine mammal: implications for conservation and maternal phylogeny of Steller sea lions (Eumetopias jubatus). Journal of Mammalogy 77:95-108.CrossRefGoogle Scholar
  3. Boily F, Beaudoin S, Measures LN (2006) Hematology and serum chemistry of harp (Phoca groenlandica) and hooded seals (Cystophora cristata) during the breeding season, in the Gulf of St. Lawrence, Canada. Journal of Wildlife Diseases 42:115-132.PubMedCrossRefGoogle Scholar
  4. Bossart GD (2006) Case study: Marine mammals as sentinel species for oceans and human health. Oceanography 19:134-137.CrossRefGoogle Scholar
  5. Bossart GD, Reidarson T, Dierauf LA, Duffield DA (2001) Clinical Pathology. In: Handbook of Marine Mammal Medicine, 2nd ed., Dierauf LA, Gulland FMD (editors), Boca Raton: CRC Press, pp 383–436Google Scholar
  6. Bowen L, Aldridge B, Beckmen K, Gelatt T, Rea L, Burek K, Pitcher K, Stott JL (2006) Differential expression of immune response genes in Steller sea lions (Eumetopias jubatus): an indicator of ecosystem health? EcoHealth 3:109-113.CrossRefGoogle Scholar
  7. Box GEP, Cox DR (1964) An analysis of transformations. Journal of the Royal Statistical Society B26:211-252.Google Scholar
  8. Braham HW, Everitt RD, Rugh DG (1980) Northern sea lion decline in the eastern Aleutian Islands. Journal of Wildlife Management 44:25-33.CrossRefGoogle Scholar
  9. Brandon EAA, Calkins DJ, Loughlin TR, Davis RW (2005) Neonatal growth of Steller sea lion (Eumetopias jubatus) pups in Alaska. Fishery Bulletin 103:246-257.Google Scholar
  10. Burek KA, Gulland FMD, O’Hara TM (2008) Effects of climate change on Arctic marine mammal health. Ecological Applications 18:S126-S134.PubMedCrossRefGoogle Scholar
  11. Burek KA, Gulland FMD, Sheffield G, Beckmen KB, Keyes E, Spraker TR, Smith AW, Skilling DE, Evermann JF, Stott JL, Saliki JT, Trites AW (2005) Infectious disease and the decline of Steller sea lions (Eumetopias jubatus) in Alaska, USA: insights from serologic data. Journal of Wildlife Diseases 41:512-524.PubMedCrossRefGoogle Scholar
  12. Calkins DG, Goodwin EA (1988) Investigation of the declining sea lion population in the Gulf of Alaska. Unpublished Report, Alaska Department of Fish and Game, Anchorage, AK, USA.Google Scholar
  13. Call KA, Loughlin TR (2005) An ecological classification of Alaskan Steller sea lion (Eumetopias jubatus) rookeries: a tool for conservation/management. Fisheries Oceanography 14:212-222.CrossRefGoogle Scholar
  14. Castellini JM, Rea LD, Lieske CL, Beckmen KB, Fadely BS, Maniscalco JM, O’Hara TM (2012) Mercury concentrations in hair from neonatal and juvenile Steller sea lions (Eumetopias jubatus): implications based on age and region in this northern Pacific marine sentinel piscivore. EcoHealth 9:267-277.PubMedCrossRefGoogle Scholar
  15. Castellini MA, Davis RW, Loughlin TR, Williams TM (1993) Blood chemistries and body composition of Steller sea lion pups at Marmot Island, Alaska. Marine Mammal Science 9:202-208.CrossRefGoogle Scholar
  16. DeMaster D (2012) Results of Steller sea lion surveys in Aleutian Islands, Alaska, June 2012. AFSC memorandum.
  17. Fadely BS, (1997) Investigations of harbor seal (Phoca vitulina) health status and body condition in the Gulf of Alaska. Ph.D. Dissertation, University of Alaska Fairbanks, Fairbanks, AK, USA.Google Scholar
  18. Fadely BS, Gelatt TS, Rea LD, King JC, Loughlin TR (2004) Geographic differences among juvenile Steller sea lion (Eumetopias jubatus) growth rates in Alaska (pp. 567–568). In: Marine Mammals of the Holarctic: Collection of Scientific Reports After the Third International Conference, Belkovich VM, Smelova IVJ, Boltunov AN (compilers), Koktebel, Crimea, Ukraine, October 11–17, 2004, Moscow: KMK.Google Scholar
  19. Fair PA, Becker PR (2000) Review of stress in marine mammals. Journal of Aquatic Ecosystem Stress and Recovery 7:335-354.CrossRefGoogle Scholar
  20. Freeman MF, Tukey JW (1950) Transformations related to the angular and the square root. Annals of Mathematical Statistics 21:607-611.CrossRefGoogle Scholar
  21. Fritz LW, Ferrero RC, Berg RJ (1995) The threatened status of Steller sea lions, Eumetopias jubatus, under the Endangered Species Act: effects on Alaska groundfish fisheries management. Marine Fisheries Review 57:14-27.Google Scholar
  22. Fritz LW, Hinckley S (2005) A critical review of the regime shift -“junk food”- hypothesis for the decline of the western stock of Steller sea lion. Marine Mammal Science 21:476-518.CrossRefGoogle Scholar
  23. Fritz L, Lynn M, Kunisch E, Sweeney K (2008) Aerial, ship, and land-based surveys of Steller sea lions (Eumetopias jubatus) in Alaska, June and July 2005 and 2007. U.S. Dep. Commer., NOAA Tech Memo., NMFS-AFSC-183.Google Scholar
  24. Fritz L, Sweeney K, Johnson D, Lynn M, Gelatt T, Gilpatrick J (2013) Aerial and ship-based surveys of Steller sea lions (Eumetopias jubatus) conducted in Alaska in June–July 2008 through 2012, and an update on the status and trend of the western distinct population segment in Alaska. U.S. Dep. Commer., NOAA Tech Memo., NMFS-AFSC-251.Google Scholar
  25. Fujino K (1960) Immunogenetic and marking approaches to identifying subpopulations of the north Pacific whales. The Scientific Reports of the Whales Research Institute 15:85-142.Google Scholar
  26. Goldstein T, Gill VA, Tuomi P, Monson D, Burdin A, Conrad PA, Dunn JL, Field C, Johnson C, Jessup DA, Bodkin J, Doroff AM (2011) Assessment of clinical pathology and pathogen exposure in sea otters (Enhydra lutris) bordering the threatened population in Alaska. Journal of Wildlife Diseases 47:579-92.PubMedCrossRefGoogle Scholar
  27. Goldstein T, Mazet JAK, Gill VA, Doroff AM, Burek KA, Hammond JA (2009) Phocine distemper virus in northern sea otters in the Pacific Ocean, Alaska, USA. Emerging Infectious Diseases 15:925-927.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Greig DJ, Gulland FMD, Rios CA, Hall AJ (2010) Hematology and serum chemistry in stranded and wild caught harbor seals in central California: reference intervals, predictors of survival, and parameters affecting blood variables. Journal of Wildlife Diseases 46:1172-1184.PubMedCrossRefGoogle Scholar
  29. Gulland FMD, Hall AJ (2005) The role of infectious disease in influencing status and trends. In: Marine Mammal Research: Conservation Beyond Crisis. Reynolds III, JE (editor), Baltimore: Johns Hopkins University Press, pp 47-61.Google Scholar
  30. Gulland FMD, Hall AJ (2007) Is marine mammal health deteriorating? Trends in the global reporting of marine mammal disease. EcoHealth 4:135-150.CrossRefGoogle Scholar
  31. Hall AJ (1998) Blood chemistry and hematology of gray seal (Halichoerus grypus) pups from birth to postweaning. Journal of Zoo and Wildlife Medicine 29:401-407.PubMedGoogle Scholar
  32. Hall AJ, Gulland FMD, Hammond JA, Schwacke LH (2010) Epidemiology, disease, and health assessment. In: Marine Mammal Ecology and Conservation, Boyd IL, Bowen WD, Iverson SJ (editors), New York: Oxford University Press, pp 144-164.Google Scholar
  33. Heath RB, Delong R, Jameson V, Brandley D, Spraker T (1997) Isoflurane anesthesia in free ranging sea lion pups. Journal of Wildlife Diseases 33:206-210.PubMedCrossRefGoogle Scholar
  34. Horn PS, Feng L, Li Y, Pesce AJ (2001) Effects of outliers and nonhealthy individuals on reference interval estimation. Clinical Chemistry 47:2137-2145.PubMedGoogle Scholar
  35. Hosseinalizadeh M, Rivaz F, Hedayatizadeh R (2011) Importance of outlier detection in spatial analysis of wind erosion. Procedia Environmental Sciences 7:341-346.CrossRefGoogle Scholar
  36. Iglewicz B, Hoaglin DC (1993) How to detect and handle outliers. Milwaukee: ASQC Quality Press.Google Scholar
  37. Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010) Hematology of southern Beaufort Sea polar bears (2005-2007): biomarker for an Arctic ecosystem health sentinel. EcoHealth 7:307-320.PubMedCrossRefGoogle Scholar
  38. Lassen ED (2004) Perspectives in data interpretation. In: Veterinary Hematology and Clinical Chemistry, Thrall MA (editor), Philadelphia: Lippincott Williams and Wilkins, pp 45-54.Google Scholar
  39. Loughlin TR (1997) Using the phylogeographic method to identify Steller sea lion stocks. In: Molecular Genetics of Marine Mammals. Dizon AE, Chivers SJ, Perrin WF (editors). Society for Marine Mammalogy Special Publication 3:159-171.Google Scholar
  40. Loughlin TR (1998) The Steller sea lion: a declining species. Biosphere Conservation 1:91-98.Google Scholar
  41. Loughlin TR, York AE (2000) An accounting of the sources of Steller sea lion, Eumetopias jubatus, mortality. Marine Fisheries Review 62:40–45.Google Scholar
  42. Mazzocchi M (2008) Statistics for marketing and consumer research. Thousand Oaks: SAGE Publications, Inc.Google Scholar
  43. Merrick RL, Brown R, Calkins DG, Loughlin TR (1995) A comparison of Steller sea lion, Eumetopias jubatus, pup masses between rookeries with increasing and decreasing populations. Fishery Bulletin 93:753-758.Google Scholar
  44. Merrick RL, Loughlin TR, Calkins DG (1987) Decline in abundance of the northern sea lion, Eumetopias jubatus, in Alaska, 1956-86. Fishery Bulletin 85:351-365.Google Scholar
  45. Moore SE (2008) Marine mammals as ecosystem sentinels. Journal of Mammalogy 89:534-540.CrossRefGoogle Scholar
  46. National Marine Fisheries Service (NMFS) (2008) Recovery Plan for the Steller sea lion (Eumetopias jubatus). Revision. National Marine Fisheries Service, Silver Spring, MD, USA.Google Scholar
  47. National Marine Fisheries Service (NMFS) (2010) Bering Sea and Aleutian Islands (BSAI) and Gulf of Alaska (GOA) Groundfish Fisheries Section 7 Consultation—Draft Biological Opinion. National Marine Fisheries Service, Alaska Region.Google Scholar
  48. National Marine Fisheries Service (NMFS) (2013) Status Review of the Eastern Distinct Population Segment of Steller Sea Lion (Eumetopias jubatus). National Marine Fisheries Service, Alaska Region.Google Scholar
  49. National Research Council (NRC) (2003) Decline of the Steller sea lion in Alaskan Waters: Untangling Food Webs and Fishing Nets. Washington DC: The National Academies Press.Google Scholar
  50. Neely BA, Soper JL, Greig DJ, Carlin KP, Favre EG, Gulland FMD, Almeida JS, Janech MG (2012) Serum profiling by MALDI-TOF mass spectrometry as a diagnostic tool for domoic acid toxicosis in California sea lions. Proteome Science 10:18.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Norman SA, Goertz CEC, Burek KA, Quakenbush LT, Cornick LA, Romano TA, Spoon T, Miller W, Beckett LA, Hobbs RC (2012) Seasonal hematology and serum chemistry of wild beluga whales (Delphinapterus leucas) in Bristol Bay, Alaska, USA. Journal of Wildlife Diseases 48:21-32.PubMedCrossRefGoogle Scholar
  52. O’Corry-Crowe G (2006) Demographic independence along ecosystem boundaries in Steller sea lions revealed by mtDNA analysis: implications for management of an endangered species. Canadian Journal of Zoology 84:1796-1809.CrossRefGoogle Scholar
  53. Phillips CD, Bickham JW, Patton JC, Gelatt TS (2009) Systematics of Steller sea lions (Eumetopias jubatus): subspecies recognition based on concordance of genetics and morphometrics. Occasional Papers, Museum of Texas Tech University 283:1-15.Google Scholar
  54. Phillips CD, Gelatt TS, Patton JC, Bickham JW (2011) Phylogeography of Steller sea lions: relationships among climate change, effective population size, and genetic diversity. Journal of Mammalogy 92:1091-1104.CrossRefGoogle Scholar
  55. Pitcher KW, Burkanov NV, Calkins DG, Le Boeuf BJ, Mamaev EG, Merrick RL, Pendleton GW (2001) Spatial and temporal variation in the timing of births of Steller sea lions. Journal of Mammalogy 82:1047-1053.CrossRefGoogle Scholar
  56. 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. Fishery Bulletin 107:102-115.Google Scholar
  57. R Development Core Team (2006) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
  58. Rapport DJ, Costanza R, McMicharl AJ (1998) Assessing ecosystem health. Trends in Ecology and Evolution 13:397-402.PubMedCrossRefGoogle Scholar
  59. Rapport DJ, Regier HA, Hutchinson TC (1985) Ecosystem behavior under stress. The American Naturalist 125:617-640.CrossRefGoogle Scholar
  60. Rea LD, Castellini JM, Correa L, Fadley BS, and O’Hara TM (2013) Maternal Steller sea lion diets elevate fetal mercury concentrations in an area of population decline. Science of the Total Environment 454-455:277-282.PubMedCrossRefGoogle Scholar
  61. Rea LD, Castellini MA, Fadley BS, Loughlin TR (1998) Health status of young Alaska Steller sea lion pups (Eumetopias jubatus) as indicated by blood chemistry and hematology. Comparative Biochemistry and Physiology Part A 120:617-623.CrossRefGoogle Scholar
  62. Rea LD, Pitcher K, Farley S, Richmond J, Dunlap-Harding W, Fadely B (2009) Percent total body lipid content increases in Steller sea lion (Eumetopias jubatus) pups during the first year of life in a similar pattern to other otariid species. In: Alaska Marine Science Symposium. January 19–23, 2009, Anchorage, AK, USA.Google Scholar
  63. Reddy ML, Dierauf LA, Gulland FMD (2001) Marine mammals as sentinels of ocean health. In: Handbook of Marine Mammal Medicine, 2nd ed., Dierauf LA, Gulland FMD (editors), Boca Raton: CRC Press, pp 3–13Google Scholar
  64. Reif JS, Bachand A, Aguirre AA, Borjesson DL, Kashinksky L, Braun R, Antonelis G (2004) Morphometry, hematology and serum chemistry in the Hawaiian monk seal (Monachus schauinslandi). Marine Mammal Science 20:851-860.CrossRefGoogle Scholar
  65. Richmond JP, Burns JM, Rea LD, Mashburn KL (2005) Postnatal ontogeny of erythropoietin and hematology in free-ranging Steller sea lions (Eumetopias jubatus). General and Comparative Endocrinology 141:240-247.PubMedCrossRefGoogle Scholar
  66. Rosen DAS, Hastie GD, Trites AW (2004) Searching for stress: hematologic indicators of nutritional inadequacies in Steller sea lions. In: Proceedings of the Comparative Nutrition Society, pp. 145–149Google Scholar
  67. Schwacke LH, Hall AJ, Townsend FI, Wells RS, Hansen LJ, Hohn AA, Bossart GD, Fair PA, Rowles TK (2009) Hematologic and serum biochemical reference intervals for free-ranging common bottlenose dolphins (Tursiops truncatus) and variation in the distributions of clinicopathologic values related to geographic sampling site. American Journal of Veterinary Research 70:973-985.PubMedCrossRefGoogle Scholar
  68. Sinclair EH, Zeppelin TK (2002) Seasonal and spatial differences in diet in the western stock of Steller sea lions. Journal of Mammalogy 83:973-990.CrossRefGoogle Scholar
  69. Solberg H (1983) The theory of reference values. Part 5. Statistical treatment of collected reference values. Determination of reference limits. Journal of Clinical Chemistry and Clinical Biochemistry 21:749-760.Google Scholar
  70. Solberg HE (2004) The IFCC recommendation of estimation of reference intervals: The RefVal Program. Clinical Chemistry and Laboratory Medicine 42:710-714.PubMedCrossRefGoogle Scholar
  71. Stockham SL, Scott MA (2002) Fundamentals of veterinary clinical pathology. Ames: Iowa State University Press.Google Scholar
  72. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540-1542.PubMedCrossRefGoogle Scholar
  73. Trumble SJ, Castellini MA (2002) Blood chemistry, hematology, and morphology of wild harbor seal pups in Alaska. Journal of Wildlife Management 66:1197-1207.CrossRefGoogle Scholar
  74. Tukey JW (1977) Exploratory Data Analysis. Addison-Wesley, Reading, MA.Google Scholar
  75. Tweedie MCK (1984) An index which distinguishes between some important exponential families. In: Statistics: Applications and New Directions. Ghosh JK, Roy J (editors). Proceedings of the Indian Statistical Institute Golden Jubilee International Conference. Calcutta, India, pp 579–604Google Scholar
  76. Watnick S, Morrison G (2005) Kidney. In: Current medical diagnosis and treatment, Tierney LM, McPhee SJ, Papadicks MA (editors), New York: McGraw-Hill, pp 867-899.Google Scholar
  77. Weiser G, Allison RW (2012) Perspectives in laboratory data interpretation and disease diagnosis. In: Veterinary Hematology and Clinical Chemistry, 2nd ed., Thrall MA, Weiser G, Allison R, Campbell T (editors), Ames: Wiley-Blackwell, pp 40–50Google Scholar
  78. Wells RS, Rhinehart HL, Hansen LJ, Sweeney JC, Townsend FI, Stone R, Casper DR, Scott MD, Hohn AA, Rowles TK (2004) Bottlenose dolphins as marine ecosystem sentinels: developing a health monitoring system. EcoHealth 1: 246-254.CrossRefGoogle Scholar
  79. Witherell D, Pautzke C, Fluharty D (2000) An ecosystem-based approach for Alaska groundfish fisheries. ICES Journal of Marine Science 57:771-777.CrossRefGoogle Scholar
  80. York AE, Merrick RL, Loughlin TR (1996) An analysis of the Steller sea lion Metapopulation in Alaska. In: Metapopulations and Wildlife Conservation, McCullough DR (editor), Washington DC: Island Press, pp 259-292.Google Scholar

Copyright information

© International Association for Ecology and Health 2014

Authors and Affiliations

  • Michelle E. Lander
    • 1
    Email author
  • Brian S. Fadely
    • 1
  • Thomas S. Gelatt
    • 1
  • Lorrie D. Rea
    • 2
  • Thomas R. Loughlin
    • 1
    • 3
  1. 1.National Marine Mammal LaboratoryAlaska Fisheries Science Center, National Marine Fisheries ServiceSeattleUSA
  2. 2.Division of Wildlife ConservationAlaska Department of Fish and GameJuneauUSA
  3. 3.TRL Wildlife ConsultingRedmondUSA

Personalised recommendations