Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Age and growth of the white shark, Carcharodon carcharias, in the western North Atlantic Ocean

Lisa J. Natanson A C and Gregory B. Skomal B

A National Marine Fisheries Service, Northeast Fisheries Science Center, NOAA, 28 Tarzwell Drive, Narragansett, RI 02882-1199, USA.

B Massachusetts Division of Marine Fisheries, 1213 Purchase Street, New Bedford, MA 02740, USA.

C Corresponding author. Email: lisa.natanson@noaa.gov

Marine and Freshwater Research 66(5) 387-398 http://dx.doi.org/10.1071/MF14127
Submitted: 10 May 2014  Accepted: 7 August 2014   Published: 6 January 2015

Abstract

Age and growth estimates for the white shark (Carcharodon carcharias) in the western North Atlantic Ocean (WNA) were derived from band pair counts on the vertebral centra of 81 specimens collected between 1963 and 2010. We used two previously published criteria to interpret band pairs and assessed the validity of each method using Δ14C levels from a recent bomb radiocarbon validation study and existing Δ14C reference chronologies in the WNA. Although both criteria produced age estimates consistent, to varying degrees, with different reference chronologies, only one was considered valid when life history information was used to select the appropriate reference chronology and minimum/maximum ages based on bomb carbon values were taken into consideration. These age estimates, validated up to 44 years, were used to develop a growth curve for the species, which was best described using the Schnute general model (sexes combined). These results indicate that white sharks grow more slowly and live longer than previously thought.

Additional keywords: carbon-14, lamnid, vertebral column.


References

Akaike, H. (1973). Information theory and the extension of the maximum likelihood principle. In ‘International Symposium on Information Theory’. (Eds B. N. Petrov and F. Csaki.) pp. 267–281. (Academiai Kaido: Budapest.)

Andrews, A. H., Natanson, L. J., Kerr, L. A., Burgess, G. H., and Cailliet, G. M. (2011). Bomb radiocarbon and tag-recapture dating of sandbar shark (Carcharhinus plumbeus). Fishery Bulletin 109, 454–465. open url image1

Ardizzone, D., Cailliet, G. M., Natanson, L. J., Kerr, L. A., and Brown, T. A. (2006). Application of bomb radiocarbon chronologies to shortfin mako (Isurus oxyrinchus) age validation. Environmental Biology of Fishes 77, 355–366.
Application of bomb radiocarbon chronologies to shortfin mako (Isurus oxyrinchus) age validation.CrossRef | open url image1

Baty, F. and Delignette-Muller, M. L. (2011). nlstools: tools for nonlinear regression diagnostics. R package version 0.0-11. Available at http://www.inside-r.org/packages/nlstools/versions/0-0-11 [Verified 9 December 2014].

Beamish, R. J., and Fournier, D. A. (1981). A method for comparing the precision of a set of age determinations. Canadian Journal of Fisheries and Aquatic Sciences 38, 982–983.
A method for comparing the precision of a set of age determinations.CrossRef | open url image1

Bigelow, H. B., and Schroeder, W. C. (1948). Sharks. In ‘Fishes of the Western North Atlantic. Part One. Lancelets, Cyclostomes, Sharks’. (Eds J. Tee-Van, C. M. Breder, S. F. Hildebrand, A. E. Parr and W. C. Schroeder.) pp. 59–546. (Sears Foundation for Marine Research, Yale University: New Haven, CT.)

Bishop, S. D. H., Francis, M. P., Duffy, C., and Montgomery, J. C. (2006). Age, growth, maturity, longevity and natural mortality of the shortfin mako (Isurus oxyrinchus) in New Zealand waters. Marine and Freshwater Research 57, 143–154.
Age, growth, maturity, longevity and natural mortality of the shortfin mako (Isurus oxyrinchus) in New Zealand waters.CrossRef | open url image1

Bowker, A. H. (1948). A test for symmetry in contingency tables. Journal of the American Statistical Association 43, 572–574.
A test for symmetry in contingency tables.CrossRef | 1:STN:280:DyaH1M%2FisVKluw%3D%3D&md5=bed69164ae3d8d40c3fa06b50932413fCAS | 18123073PubMed | open url image1

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information – Theoretic Approach’, 2nd edn. (Springer: New York.)

Cailliet, G. M. (1990). Elasmobranch age determination and verification: an updated review. In ‘Elasmobranchs as Living Resources’. Technical Report NMFS 90. (Eds H. L. Pratt Jr, S. H. Gruber, and T. Taniuchi.) pp. 157–165. (NOAA: Silver Spring, MD.)

Cailliet, G. M., and Goldman, K. J. (2004). Age determination and validation in chondrichthyan fishes. In ‘The Biology of Sharks and Their Relatives, Vol. 1.’ (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 399–447 (CRC Press: Boca Raton, FL.)

Cailliet, G. M., Natanson, L. J., Welden, B. A., and Ebert, D. A. (1985). Preliminary studies on the age and growth of the white shark, Carcharodon carcharias, using vertebral bands. In ‘Biology of the White Shark’, Memoirs of the Southern California Academy of Science, vol. 9. (Eds J. A. Seigal and C. C. Swift.) pp. 49–60. (Southern California Academy of Sciences: Los Angeles, CA.)

Campana, S. E., Annand, M. C., and McMillan, J. I. (1995). Graphical methods for determining the consistency of age determinations. Transactions of the American Fisheries Society 124, 131–138.
Graphical methods for determining the consistency of age determinations.CrossRef | open url image1

Campana, S. E., Natanson, L. J., and Myklevoll, S. (2002). Bomb dating and age determination of a large pelagic shark. Canadian Journal of Fisheries and Aquatic Sciences 59, 450–455.
Bomb dating and age determination of a large pelagic shark.CrossRef | open url image1

Carey, F. G., Kanwisher, J. W., Brazier, O., Gabrielsen, G., Casey, J. G., and Pratt, H. L. (1982). Temperature and activities of a white shark, Carcharodon carcharias. Copeia 1982, 254–260.
Temperature and activities of a white shark, Carcharodon carcharias.CrossRef | open url image1

Casey, J. G., and Pratt, H. L. (1985). Distribution of the white shark (Carcharodon carcharias) in the western North. Memoirs of the Southern California Academy of Science 9, 2–14. open url image1

Casey, J. G., Pratt, H. L., and Stillwell, C. E. (1985). Age and growth of the sandbar shark (Carcharhinus plumbeus) from the western North Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 42, 963–975.
Age and growth of the sandbar shark (Carcharhinus plumbeus) from the western North Atlantic.CrossRef | open url image1

Compagno, L. J. V. (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 2(1). (FAO: Rome.)

Curtis, T., McCandless, C. T., Carlson, J. K., Skomal, G. B., Kohler, N. E., Natanson, L. J., Burgess, G. H., Hoey, J. J., and Pratt, H. L. (2014). Seasonal distribution and historic trends of white sharks, Carcharodon carcharias, in the western North Atlantic Ocean. PLoS ONE 9, e99240.
Seasonal distribution and historic trends of white sharks, Carcharodon carcharias, in the western North Atlantic Ocean.CrossRef | 24918579PubMed | open url image1

Evans, G. T., and Hoenig, J. M. (1998). Testing and viewing symmetry in contingency tables, with applications to readers of fish ages. Biometrics 54, 620–629.
Testing and viewing symmetry in contingency tables, with applications to readers of fish ages.CrossRef | open url image1

Francis, M. P. (1996). Observations on a pregnant white shark with a review of reproductive biology. In ‘Great White Sharks: The Biology of Carcharodon carcharias’. (Eds A. P. Klimley, and D. G. Ainley.) pp. 157–172. (Academic Press: San Diego, CA.)

Francis, M. P., Campana, S., and Jones, C. M. (2007). Age underestimation in New Zealand porbeagle sharks (Lamna nasus): is there an upper limit to ages that can be determined from shark vertebrae? Marine and Freshwater Research 58, 10–23.
Age underestimation in New Zealand porbeagle sharks (Lamna nasus): is there an upper limit to ages that can be determined from shark vertebrae?CrossRef | open url image1

Goldman, K. J., Cailliet, G. M., Andrews, A. H., and Natanson, L. J. (2012). Assessing the age and growth of chondrichthyan fishes. In ‘Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 423–451. (CRC Press LLC: New York.)

Hamady, L. L. (2014). Age, movements, and feeding ecology of Northwest Atlantic white sharks estimated from ecogeochemical profiles in vertebrae. Ph.D. Thesis. Woods Hole Oceanographic Institution, MA, USA.

Hamady, L. L., Thorrold, S., and Natanson, L. J. (2014). Bomb carbon age validation of the white shark, Carcharodon carcharias, in the western North Atlantic Ocean. PLoS ONE 9, e84006.
Bomb carbon age validation of the white shark, Carcharodon carcharias, in the western North Atlantic Ocean.CrossRef | 24416189PubMed | open url image1

Hoenig, J. M., Morgan, M. J., and Brown, C. A. (1995). Analyzing differences between two age determination methods by tests of symmetry. Canadian Journal of Fisheries and Aquatic Sciences 52, 364–368.
Analyzing differences between two age determination methods by tests of symmetry.CrossRef | open url image1

Kalish, J. M., and Johnston, J. (2001). Determination of school shark age based on analysis of radiocarbon in vertebral collagen. In ‘Use of the Bomb Radiocarbon Chronometer to Validate Fish Age: Final Report, FDRC Project 93/109’. (Ed. J. M. Kalish.) pp. 116–122. (Fisheries Research and Development Corporation: Canberra, ACT.)

Kerr, L. A., Andrews, A. H., Cailliet, G. M., Brown, T. A., and Coale, K. H. (2006). Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environmental Biology of Fishes 77, 337–353.
Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean.CrossRef | open url image1

Kneebone, J., Natanson, L. J., Andrews, A. H., and Howell, W. H. (2008). Using bomb radiocarbon analyses to validate age and growth estimates for the tiger shark, Galeocerdo cuvier, in the western North Atlantic. Marine Biology 154, 423–434.
Using bomb radiocarbon analyses to validate age and growth estimates for the tiger shark, Galeocerdo cuvier, in the western North Atlantic.CrossRef | open url image1

Kohler, N. E., Casey, J. G., and Turner, P. A. (1996). Length-length and length-weight relationships for 13 species of sharks from the western North Atlantic. NOAA Technical Report Memorandum (NMFS-NE-110.) (NOAA: Silver Spring, MD.)

McNemar, Q. (1947). Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika 12, 153–157.
Note on the sampling error of the difference between correlated proportions or percentages.CrossRef | 1:STN:280:DyaH2s%2Fhs1aksA%3D%3D&md5=8b51c66d1705eb89fceb757dcf0b9234CAS | 20254758PubMed | open url image1

Mollet, H. F., and Cailliet, G. M. (2002). Comparative population demography of elasmobranchs using life history tables, Leslie matrices and stage-based matrix models. Marine and Freshwater Research 53, 503–516.
Comparative population demography of elasmobranchs using life history tables, Leslie matrices and stage-based matrix models.CrossRef | open url image1

Natanson, L. J., and Cailliet, G. M. (1990). Vertebral growth zone deposition in Pacific angel sharks. Copeia 1990, 1133–1145.
Vertebral growth zone deposition in Pacific angel sharks.CrossRef | open url image1

Natanson, L. J., Mello, J. J., and Campana, S. E. (2002). Validated age and growth of the porbeagle shark (Lamna nasus) in the western North Atlantic Ocean. Fishery Bulletin 100, 266–278. open url image1

Natanson, L. J., Ardizzone, D., Cailliet, G. M., Wintner, S., and Mollet, H. (2006). Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean. Environmental Biology of Fishes 77, 367–383.
Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean.CrossRef | open url image1

Natanson, L. J., Wintner, S. P., Johansson, F., Piercy, A., Campbell, P., De Maddalena, A., Gulak, S. J. B., Human, B., Cigala Fulgosi, F., Ebert, D. A., Fong, J. D., Hemida, F., Mollen, F. H., Vanni, S., Burgess, G. H., Compagno, L. J. V., and Wedderburn-Maxwell, A. (2008). Preliminary investigation of vertebral band pairs in the basking shark Cetorhinus maximus (Gunnerus). Marine Ecology Progress Series 361, 267–278.
Preliminary investigation of vertebral band pairs in the basking shark Cetorhinus maximus (Gunnerus).CrossRef | open url image1

Natanson, L. J., Gervelis, B. J., Winton, M. V., Hamady, L. L., Gulak, S. J. B., and Carlson, J. K. (2014). Validated age and growth estimates for Carcharhinus obscurus in the northwestern Atlantic Ocean, with pre- and post management growth comparisons. Environmental Biology of Fishes 97, 881–896.
Validated age and growth estimates for Carcharhinus obscurus in the northwestern Atlantic Ocean, with pre- and post management growth comparisons.CrossRef | open url image1

NMFS (1999) ‘Final Fishery Management Plan for Atlantic Tuna, Swordfish, and Sharks.’ (National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Office of Sustainable Fisheries, Highly Migratory Species Management Division, Silver Spring, MD.)

Passerotti, M. S., Andrews, A. H., Carlson, J. K., Wintner, S. P., Goldman, K. J., and Natanson, L. J. (2014). Maximum age and missing time in the vertebrae of sand tiger shark (Carcharias taurus): validated lifespan from bomb radiocarbon dating in the western North Atlantic and southwestern Indian Oceans. Marine and Freshwater Research , .
Maximum age and missing time in the vertebrae of sand tiger shark (Carcharias taurus): validated lifespan from bomb radiocarbon dating in the western North Atlantic and southwestern Indian Oceans.CrossRef | open url image1

Pratt, H. L. (1996). Reproduction in the male white shark. In ‘Great White Sharks: the Biology of Carcharodon carcharias’. (Eds A. P. Klimley, and D. G. Ainley.) pp. 131–138. (Academic Press: San Diego, CA.)

Pratt, H. L., Casey, J. G., and Conklin, R. B. (1982). Observations on large white sharks, Carcharodon carcharias, off Long Island, New York. Fishery Bulletin 80, 153–156. open url image1

R Development Core Team (2010). R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.)

Ricker, W. E. (1975). Computations and interpretation of biological statistics of fish populations. Bulletin of the Fisheries Research Board Canada 191, 1–382. open url image1

Ricker, W. E. (1979). Growth rates and models. In ‘Fish Physiology Vol. VIII: Bioenergetics and Growth’. (Eds. W. S. Hoar, D. J. Randall, and J. R. Brett.), pp. 677–743. (Academic Press: New York.)

Ridewood, W. G. (1921). On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of Biological Sciences 210, 311–407.
On the calcification of the vertebral centra in sharks and rays.CrossRef | open url image1

Schnute, J. (1981). A versatile growth model with statistically stable parameters. Canadian Journal of Fisheries and Aquatic Sciences 38, 1128–1140.
A versatile growth model with statistically stable parameters.CrossRef | open url image1

Skomal, G. B., and Natanson, L. J. (2003). Age and growth of the blue shark (Prionace glauca) in the North Atlantic Ocean. Fishery Bulletin 101, 627–639. open url image1

Skomal, G. B., Chisholm, J., and Correia, S. J. 2012. Implications of increasing pinniped populations on the diet and abundance of white sharks off the coast of Massachusetts. In ‘Global Perspectives on the Biology and Life History of the Great White Shark’. (Ed. M. L. Domeier.) pp. 405–418. (CRC Press: Boca Raton, FL.)

Stevens, J. D., Bonfil, R., Dulvy, N. K., and Walker, P. A. (2000). The effects of fishing on sharks, rays, and chimaeras (Chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.
The effects of fishing on sharks, rays, and chimaeras (Chondrichthyans), and the implications for marine ecosystems.CrossRef | open url image1

Tanaka, S. T., Kitamura, T., Mochizuki, T., and Kofuji, K. (2011). Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kashima-nada. Marine and Freshwater Research 62, 548–556.
Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kashima-nada.CrossRef | 1:CAS:528:DC%2BC3MXnvFanu7c%3D&md5=bbcd270cdabef85f653e45a85da4a597CAS | open url image1

Templeman, W. (1963). Distribution of sharks in the Canadian Atlantic (with special reference to Newfoundland waters). Journal of the Fisheries Research Board of Canada 140, 1–77. open url image1

Uchida, S., Toda, M., Teshima, K., and Yano, K. (1996) Pregnant white sharks and full-term embryos from Japan. In ‘Great White Sharks: The Biology of Carcharodon carcharias’. (Eds A. P. Klimley, and D. G. Ainley.) pp. 139–156. (Academic Press, San Diego, CA.)

von Bertalanffy, L. (1938). A quantitative theory of organic growth (inquiries on growth laws II). Human Biology 10, 181–213.
| 1:CAS:528:DyaA1MXksVGhtg%3D%3D&md5=c4514509487e661924366bfdcba62676CAS | open url image1

Wintner, S. P., and Cliff, G. (1999). Age and growth determination of the white shark, Carcharodon carcharias, from the east coast of South Africa. Fishery Bulletin 97, 153–169. open url image1



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