Skip to main content
Log in

Investigations of Δ 14C, δ 13C, and δ 15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean

  • ELASMOBRANCHS
  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The white shark, Carcharodon carcharias, has a complex life history that is characterized by large scale movements and a highly variable diet. Estimates of age and growth for the white shark from the eastern North Pacific Ocean indicate they have a slow growth rate and a relatively high longevity. Age, growth, and longevity estimates useful for stock assessment and fishery models, however, require some form of validation. By counting vertebral growth band pairs, ages can be estimated, but because not all sharks deposit annual growth bands and many are not easily discernable, it is necessary to validate growth band periodicity with an independent method. Radiocarbon (14C) age validation uses the discrete 14C signal produced from thermonuclear testing in the 1950s and 1960s that is retained in skeletal structures as a time-specific marker. Growth band pairs in vertebrae, estimated as annual and spanning the 1930s to 1990s, were analyzed for Δ14C and stable carbon and nitrogen isotopes (δ13C and δ15N). The aim of this study was to evaluate the utility of 14C age validation for a wide-ranging species with a complex life history and to use stable isotope measurements in vertebrae as a means of resolving complexity introduced into the 14C chronology by ontogenetic shifts in diet and habitat. Stable isotopes provided useful trophic position information; however, validation of age estimates was confounded by what may have been some combination of the dietary source of carbon to the vertebrae, large-scale movement patterns, and steep 14C gradients with depth in the eastern North Pacific Ocean.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. Monterey Bay Aquarium News Release, 31 March 2005

References

  • Andrews AH, Burton EJ, Kerr LA, Cailliet GM, Coale KH, Lundstrom CC, Brown TA (2005) Bomb radiocarbon and lead-radium disequilibria in otoliths of bocaccio rockfish (Sebastes paucispinis): a determination of age and longevity for a difficult-to-age fish. Mar Freshwater Res 56:517–528

    Article  CAS  Google Scholar 

  • Ardizzone D, Cailliet GM, Natanson LJ, Andrews AH, Kerr LA, Brown TA (2006) Application of Bomb Radiocarbon Chronologies to Shortfin Mako (Isurus oxyrinchus) Age Validation. Environ Biol Fishes (this volume)

  • Bonfil R, Meyer M, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, Swanson S, Kotze D, Paterson M (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310:100–103

    Article  CAS  Google Scholar 

  • Boustany AM, Davis SF, Pyle P, Anderson SD, Le Boef BJ, Block BA (2002) Satellite tagging: expanded niche for white sharks. Nature 415:35–36

    Article  CAS  Google Scholar 

  • Broeker WS, Peng T-H (1982) The anthropogenic invasion: the movement of water through the oceanic thermocline. In: Broeker WS, Peng T-H (eds), Tracers in the sea. Lamont–Doherty Geological Observatory, New York, pp 383–444

    Google Scholar 

  • Brown TA, Nelson DE, Vogel JS, Southon JR (1988) Improved collagen extraction by modified Longin method. Radiocarbon 30(2):171–177

    CAS  Google Scholar 

  • Burton RK, Koch PL (1999) Isotopic tracking of foraging and long distance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585

    Article  Google Scholar 

  • Burton RK, Snodgrass JJ, Gifford-Gonzalez D, Guilderson T, Brown T, Koch PL (2001) Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna. Oecologia 128:107–115

    Article  Google Scholar 

  • Cailliet GM (1990) Elasmobranch age determination and verification: an updated review. In: Pratt HL Jr, Gruber SH and Taniuchi T (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics and the status of the fisheries, U.S. Department of Commerce, NOAA Tech. Rep. NMFS 90, pp 157–165

  • Cailliet GM, Goldman KJ (2004) Age determination and validation in chondrichthyan fishes. In: Carrier J, Musick JA, Heithaus MR (eds), Biology of sharks and their relatives. CRC Press LLC, Boca Raton, Florida, pp 399–447

    Google Scholar 

  • Cailliet, GM, Martin LK, Kusher D, Wolf P, Welden BA (1983) Techniques for enhancing vertebral bands in age estimation of California elasmobranchs. In: Prince ED, Pulos LM (eds) Proceedings international workshop on age determination of oceanic pelagic fishes, Tunas, Billfishes, Sharks, NOAA Tech. Rep. NMFS 8, pp 157–165

  • Cailliet GM, Natanson LJ, Welden BA, Ebert DA (1985) Preliminary studies on the age and growth of the white shark, Carcharodon carcharias, using vertebral bands. Memoirs Southern Calif Acad Sci 9:49–60

    Google Scholar 

  • Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Progr Ser 188:263–297

    CAS  Google Scholar 

  • Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242

    Article  Google Scholar 

  • Campana SE, Natanson LJ, Myklevoll S (2002) Bomb dating and age determination of large pelagic sharks. Can J Fish Aquat Sci 59:450–455

    Article  Google Scholar 

  • Chang WYB (1982) A statistical method for evaluating reproducibility of age determination. Can J Fish Aquat Sci 39:1208–1210

    Article  Google Scholar 

  • Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date, vol 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO Species Catalogue for Fishery Purposes. No. 1, vol. 2. Rome, FAO, 269 pp

  • Cortes E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45:341–351

    Article  CAS  Google Scholar 

  • Dewar H, Domeier M, Nasby-Lucas N (2004) Insights into young of the year white shark, Carcharodon carcharias, behavior in the southern California Bight. Environ Biol Fish 70(2):133–143

    Article  Google Scholar 

  • Druffel ERM, Williams PM (1990) Identification of a deep marine source of particulate organic carbon using bomb 14C. Nature 347:172–174

    Article  CAS  Google Scholar 

  • Ebert TA, Southon JR (2003) Red sea urchins (Strongylocentus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fish Bull 101:915–922

    Google Scholar 

  • Estrada JA, Rice AN, Lutcavage ME, Skomal GB (2003) Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J Mar Biol Assoc UK 83:1347–1350

    Article  CAS  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87(4):829–834

    Google Scholar 

  • Farrell J, Campana SE (1996) Regulation of calcium and strontium deposition on the otoliths of juvenile tilapia, Oreochromis niloticus. Comp Biochem Physiol 115A:103–109

    Article  CAS  Google Scholar 

  • Fisk AT, Tittlemier SA, Pranschke JL, Norstrom RJ (2002) Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of greenland sharks. Ecology 83:2162–2172

    Google Scholar 

  • France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Progr Ser 124:307–312

    Google Scholar 

  • Frantz BR, Foster MS, Riosmena-Rodriguez R (2005) Clathromorphum nereostratum (Corallinales, Rhodophyta): the oldest alga? J Phycol 41(4):770–773

    Article  Google Scholar 

  • Frantz BR, Kashgarian M, Coale KH, Foster MH (2000) Growth rate and potential climate record from a rhodolith using 14C accelerator mass spectrometry. Limnol Oceanogr 45(8):1773–1777

    Article  Google Scholar 

  • Guilderson TP, Schrag DP, Kashgarian M, Southon J (1998) Radiocarbon variability in the western equatorial Pacific inferred from a high-resolution coral record from Nauru Island. J Geophys Res 103(C11):24641–24650

    Article  CAS  Google Scholar 

  • Jarman WM, Hobson KA, Sydeman WJ, Bacon CE, McLaren EB (1996) Influence of trophic position and feeding location on contaminant levels in the Gulf of the Farallones food web revealed by stable isotope analysis. Environ Sci Technol 30(2):654–660

    Article  CAS  Google Scholar 

  • Kalish JM (1991) 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Mar Ecol Progr Ser 75:191–203

    Google Scholar 

  • Kalish JM (1995) Radiocarbon and fish biology. In: Secor DH, Dean JM, Campana SE (eds) Recent developments in fish otolith research. University of South Carolina Press, Columbia, South Carolina, pp 637–653

    Google Scholar 

  • Kalish JM, DeMartini E (2001) Determination of swordfish (Xiphias gladius) age based on analysis of radiocarbon in vertebral carbonate and collagen. In: Kalish JM (ed), Use of the bomb radiocarbon chronometer to validate fish age. Final Report FRDC Project 93/109. Fisheries Research and Development Corporation, Canberra, Australia, pp 340–351

    Google Scholar 

  • Kalish JM, Johnston J (2001) Determination of school shark age based on analysis of radiocarbon in vertebral collagen. In: Kalish JM (ed), Use of the bomb radiocarbon chronometer to validate fish age. Final Report. FDRC Project 93/109. Fisheries Research and Development Corporation, Canberra, Australia, pp 116–122

    Google Scholar 

  • Kerr LA, Andrews AH, Frantz BR, Coale KH, Brown TA, Cailliet GM (2004) Radiocarbon in otoliths of yelloweye rockfish (Sebastes ruberrimus): a reference time series for the waters of southeast Alaska. Can J Fish Aquat Sci 61:443–451

    Article  Google Scholar 

  • Kerr LA, Andrews AH, Frantz BR, Coale KH, Brown TA, Munk K, Cailliet GM (2005) Age validation of quillback rockfish (Sebastes maliger) using bomb radiocarbon. Fish Bull 103(1):97–107

    Google Scholar 

  • Klimley AP (1985) The areal distribution and autoecology of the white shark, Carcharodon carcharias, off the west coast of North America. Southern Calif Acad Sci 9:15–40

    Google Scholar 

  • Koch PL, Fogel ML, Tuross N (1994) Tracing the diet of fossil animals using stable isotopes. In: Lajtha K, Michener RH (eds), Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, New York, New York, USA, pp 63–92

    Google Scholar 

  • Le Boeuf BJ, Riedman ML, Keyes RS (1982) White shark predation on pinnipeds in California coastal waters. Fish Bull 80:891–895

    Google Scholar 

  • Michener RH, Schell DM (1994) Stable isotope rations as tracers in marine aquatic food webs. In: Michener RH, Schell DM (eds), Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, New York, New York, USA, pp 138–157

    Google Scholar 

  • Mollet HF, Cliff G, Pratt HL Jr, Stevens JD (2000) Reproductive biology of the female shortfin mako Isurus oxyrinchus Rafinesque 1810, with comments on the embryonic development of lamnoids. Fish Bull 98(2):299–318

    Google Scholar 

  • Pearcy, Stuvier (1983) Vertical transport of carbon-14 into deep-sea food webs. Deep-Sea Res 30(4A):427–440

    Article  CAS  Google Scholar 

  • Perry RI, Thompson PA, Mackas DL, Harrison PJ, Yelland DR (1999) Stable carbon isotopes as pelagic food web tracers in adjacent shelf and slope regions off British Columbia, Canada. Can J Fish Aquat Sci 56:2477–2486

    Article  CAS  Google Scholar 

  • Piner K, Wischniowski SG (2004) Pacific halibut chronology of bomb radiocarbon in otoliths from 1944 to 1981 and a validation of ageing methods. J Fish Biol 64:1060–1071

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Google Scholar 

  • Ridewood WG (1921) On the calcification of the vertebral central in sharks and rays. Philadelphia Trans Roy Soc Lond Ser B 210:311–407

    Google Scholar 

  • Schoeninger GJ, Deniro GJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica Cosmochimica Acta 48:625–639

    Article  CAS  Google Scholar 

  • Springer AM, Estes JA, van Vliet GB, Williams TM, Doak DF, Danner EM, Forney KA, Pfister B (2003) Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? Proc Nat Acad Sci 100(21):12223–12228

    Article  CAS  Google Scholar 

  • Stuvier M, Polach HA (1977) Discussion reporting of 14C data. Radiocarbon 19(3):355–363

    Google Scholar 

  • Toperoff AK (1997) Diet of harbor porpoise (P. phocoena) using stomach contents and stable isotope analyses. A thesis presented to the faculty of California State University, San Jose through Moss Landing Marine laboratories, 103 p

  • Tricas TC, McCosker JE (1984) Predatory behavior of the white shark (Carcharodon carcharias), with notes on its biology. Proc Calif Acad Sci 43:221–238

    Google Scholar 

  • Urist MR (1961) Calcium and phosphorus in the blood and skeleton of the elasmobranchii. Endocrinology 69:778–801

    Article  CAS  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ15N and δ 13C and the trophic position of aquatic consumers. Ecology 80(4):1395–1404

    Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ 15N and δ 13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46(8):2061–2066

    Article  CAS  Google Scholar 

  • Vogel JS, Nelson DE, Southon JR (1987) 14C background levels in an accelerator mass spectrometry system. Radiocarbon 29(3):323–333

    CAS  Google Scholar 

  • Vogel JS, Southon JR, Nelson DE, Brown TA (1984) Performance of catalytically condensed carbon for use in accelerator mass spectrometry. Nuclear Instrument Methods Phys Res B5:289–293

    Article  Google Scholar 

  • Welden BA, Cailliet GM, Flegal AR (1987) Comparison of radiometric with vertebral band age estimates in four California elasmobranchs. In: Summerfelt RC, Hall GE (eds), Age and growth of fish. Iowa State University Press, Ames, Iowa, pp 301–315

    Google Scholar 

  • Wintner SP, Cliff G (1999) Age and growth determination of the white shark, Carcharodon carcharias, from the east coast of South Africa. Fish Bull 97:153–169

    Google Scholar 

Download references

Acknowledgments

We thank the Los Angeles County Museum, California Academy of Sciences, Sea World San Diego, and Leonard Compagno (Shark Research Center, Iziko-Museums of Cape Town South African Museum, Cape Town, South Africa) for providing vertebral samples. We acknowledge Steve Campana, John Kalish, Sora Kim, Rob Leaf, and Rob Burton for their insights regarding these results and for improving the manuscript. We thank Lisa Natanson for her assistance in white shark vertebrae ageing. This paper was supported in part by the Pacific Shark Research Center and the National Sea Grant College Program of the U.S. Department of Commerce’s National Oceanic and Atmospheric Administration under NOAA Grant #NA06RG0142, project number R/F-190, through the California Sea Grant College Program, and in part by the California State Resources Agency. The views expressed herein do not necessarily reflect the views of any of those organizations. This work was performed, in part, under the auspices of the U.S. Department of Energy by University of California, Lawrence Livermore National Laboratory under Contract No. W-7405-Eng-48.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lisa A. Kerr.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kerr, L.A., Andrews, A.H., Cailliet, G.M. et al. Investigations of Δ 14C, δ 13C, and δ 15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environ Biol Fish 77, 337–353 (2006). https://doi.org/10.1007/s10641-006-9125-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-006-9125-1

Keywords

Navigation