Marine Biology

, 163:144 | Cite as

Using bomb radiocarbon to estimate age and growth of the white shark, Carcharodon carcharias, from the southwestern Indian Ocean

  • Heather M. ChristiansenEmail author
  • Steven E. Campana
  • Aaron T. Fisk
  • Geremy Cliff
  • Sabine P. Wintner
  • Sheldon F. J. Dudley
  • Lisa A. Kerr
  • Nigel E. Hussey
Original paper


Knowledge of age and growth parameters is vital to the conservation and management of white sharks (Carcharodon carcharias), but ages have not been validated for all populations and growth rates can vary regionally. Bomb radiocarbon (14C) analyses conducted on four individual white sharks [329, 414, 487, and 537 cm fork length (FL)] from the southwest Indian Ocean (SWI) were proximally aligned with Δ14C reference chronologies accepting established error, providing evidence to support annual band pair formation to 30–38 years for the SWI population. To enable comparison with previous studies on bomb radiocarbon in white sharks, a subset of specimens from the northwest Atlantic Ocean (NWA; 223.5, 441, and 493 cm FL) and northeast Pacific Ocean (NEP; 214, 365, and 429 cm FL) were also analyzed for 14C, revealing samples from the SWI were more enriched in 14C than samples from the NWA or NEP. Vertebral band pair counts were then determined for a larger set of white sharks from the SWI (140–422 cm FL, n = 51) resulting in age ranges of 1–38 years. The Gompertz growth model best described the SWI data, with an asymptotic size (L ) of 496.77 cm FL and length at birth (L 0) of 134.08 cm FL. The results of this study indicate white sharks in the SWI are longer-lived and grow more slowly compared to past estimates, but these data are more similar to recent age and growth estimates from other geographically distinct populations. This has important implications for the management of this species in the waters off southern Africa.


Fork Length White Shark Band Pair Vertebral Centra Carcharodon Carcharias 
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.



The Natural Science and Engineering Research Council of Canada and the Canada Research Chair program provided funding for this project to ATF. HMC was supported in part by scholarships and graduate assistantships from the University of Windsor. We thank the KwaZulu-Natal Sharks Board Laboratory and Operations staff for the dissection of sharks and sample collection and Warren Joyce from the Bedford Institute of Oceanography for preparing, imaging, and micromilling vertebral sections for bomb radiocarbon analysis. We appreciate the discussions with Lisa Natanson and thank her for her assistance with manuscript edits. We thank Megan Winton for her assistance with the statistical analysis. We also thank Allen H. Andrews of NOAA Fisheries and an anonymous reviewer for their helpful comments on the manuscript.

Supplementary material

227_2016_2916_MOESM1_ESM.pdf (55 kb)
Supplementary material 1 (PDF 55 kb)
227_2016_2916_MOESM2_ESM.pdf (66 kb)
Supplementary material 2 (PDF 66 kb)
227_2016_2916_MOESM3_ESM.pdf (88 kb)
Supplementary material 3 (PDF 87 kb)


  1. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proceedings of the second international symposium on information theory. Akademiai Kiad, Budapest, pp 267–281Google Scholar
  2. Andrews AH, Kerr LA (2015) Validated age estimates for large white sharks of the northeastern Pacific Ocean: altered perceptions of vertebral growth shed light on complicated bomb Δ14C results. Environ Biol Fish 98:971–978. doi: 10.1007/s10641-014-0326-8 CrossRefGoogle Scholar
  3. Andrews AH, Natanson LJ, Kerr LA, Burgess GH, Cailliet GM (2011) Bomb radiocarbon and tag-recapture dating of sandbar shark (Carcharhinus plumbeus). Fish Bull 109:454–465Google Scholar
  4. 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 Fish 77:355–366. doi: 10.1007/s10641-006-9106-4 CrossRefGoogle Scholar
  5. Baty F, Delignette-Muller ML (2011) nlstools: tools for nonlinear regression diagnostics. R package version 0.0-11. R Foundation for Statistical Computing, ViennaGoogle Scholar
  6. Beamish RJ, McFarlane GA (1983) The forgotten requirement for age validation in fisheries biology. Trans Am Fish Soc 112:735–743. doi: 10.1577/1548-8659(1983)112%3C735:TFRFAV%3E2.0.CO;2 CrossRefGoogle Scholar
  7. Broecker WS, Peng TH (1982) Tracers in the sea. Lamont-Doherty Geological Observatory, PalisadesGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  9. Cailliet GM, Andrews AH (2008) Age-validated longevity of fishes: its importance for sustainable fisheries. In: Tsukamoto K, Kawamura T, Takeuchi T, Beard TD Jr, Kaiser MJ (eds) Fisheries for global welfare and environment, 5th world fisheries congress. Terrapub, Tokyo, pp 103–120Google Scholar
  10. Cailliet GM, Goldman KJ (2004) Age determination and validation in chondrichthyan fishes. In: Carrier JC, Musick J, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, New York, pp 399–447Google Scholar
  11. 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. Mem S Cal Acad Sci 9:49–60Google Scholar
  12. Cailliet GM, Smith WD, Mollet HF, Goldman KJ (2006) Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting. Environ Biol Fish 77:211–228. doi: 10.1007/s10641-006-9105-5 CrossRefGoogle Scholar
  13. Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297. doi: 10.3354/meps188263 CrossRefGoogle Scholar
  14. 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. doi: 10.1111/j.1095-8649.2001.tb00127.x CrossRefGoogle Scholar
  15. Campana SE (2014) Age determination of elasmobranchs, with special reference to Mediterranean species: a technical manual. Studies and Reviews. General Fisheries Commission for the Mediterranean. No. 94. Rome, FAO 2014Google Scholar
  16. Campana SE, Natanson LJ, Myklevoll S (2002) Bomb dating and age determination of large pelagic sharks. Can J Fish Aquat Sci 59:450–455. doi: 10.1139/F02-027 CrossRefGoogle Scholar
  17. Casey JG, Pratt HL Jr, Stillwell CE (1985) Growth of the sandbar shark (Carcharhinus plumbeus) from the Western North Atlantic. Can J Fish Aquat Sci 42:963–975. doi: 10.1139/f85-121 CrossRefGoogle Scholar
  18. Cliff G, Dudley SFJ (2011) Reducing the environmental impact of shark control programs: a case study from KwaZulu-Natal, South Africa. Mar Freshw Res 62:700–709. doi: 10.1071/MF10182 CrossRefGoogle Scholar
  19. Cliff G, Dudley SFJ, Jury MR (1996a) Catches of white sharks in KwaZulu-Natal, South Africa and environmental influences. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 351–362. doi: 10.1016/B978-012415031-7/50033-1 CrossRefGoogle Scholar
  20. Cliff G, van der Elst RP, Govender A, Witthuhn TK, Bullen EM (1996b) First estimates of mortality and population size of white sharks on the South African coast. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 393–400. doi: 10.1016/B978-012415031-7/50037-9 CrossRefGoogle Scholar
  21. Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  22. Druffel ERM (1989) Decade time scale variability of ventilation in the north Atlantic: high precision measurements of bomb radiocarbon in banded corals. J Geophys Res 94:3271–3285. doi: 10.1029/JC094IC03P03271 CrossRefGoogle Scholar
  23. Druffel ERM, Linick TW (1978) Radiocarbon in annual coral rings of Florida. Geophys Res Lett 5:913–916. doi: 10.1029/GL005i011p00913 CrossRefGoogle Scholar
  24. Druffel ERM, Griffin S, Guilderson TP (2001) Changes of subtropical north Pacific radiocarbon and correlation with climate variability. Radiocarbon 43:15–25Google Scholar
  25. Dudley SFJ, Simpfendorfer CA (2006) Population status of 14 shark species caught in the protective gillnets off KwaZulu-Natal beaches, South Africa, 1978–2003. Mar Freshw Res 57:225–240. doi: 10.1071/MF05156 CrossRefGoogle Scholar
  26. Dudley SFJ, Cliff G, Zungu MP, Smale MJ (2005) Sharks caught in protective gill nets off KwaZulu-Natal, South Africa. 10. The dusky shark, Carcharhinus obscurus (Lesueur 1818). Afr J Mar Sci 17:107–127. doi: 10.2989/18142320509504072 CrossRefGoogle Scholar
  27. Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834. doi: 10.1890/0012-9658(2006)87%5B829:UOIAOV%5D2.0.CO;2 CrossRefGoogle Scholar
  28. Francis MP (1996) Observations on a pregnant white shark with a review of reproductive biology. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 157–172. doi: 10.1016/B978-012415031-7/50016-1 CrossRefGoogle Scholar
  29. Francis MP, Campana SE, Jones CM (2007) Age under-estimation in New Zealand porbeagle sharks (Lamna nasus): is there an upper limit to ages that can be determined from shark vertebrae? Mar Freshw Res 58:10–23. doi: 10.1071/MF06069 CrossRefGoogle Scholar
  30. Fry B (1988) Food web structure on Georges Bank from stable C, N and S isotopic composition. Limnol Oceanogr 33:1182–1190. doi: 10.4319/lo.1988.33.5.1182 CrossRefGoogle Scholar
  31. Goldman KJ, Cailliet GM, Andrews AH, Natanson LJ (2012) Assessing the age and growth of chondrichthyan fishes. In: Carrier J, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 423–451. doi: 10.1201/b11867-18 CrossRefGoogle Scholar
  32. Gordon AL (1986) Interocean exchange of thermocline water. J Geophys Res 91:5037–5046. doi: 10.1029/JC091IC04P05037 CrossRefGoogle Scholar
  33. Grumet NS, Guilderson TP, Dunbar RB (2002) Pre-bomb radiocarbon variability inferred from a Kenyan coral record. Radiocarbon 44:590–591Google Scholar
  34. Hamady LL, Natanson LJ, Skomal GB, Thorrold SR (2014) Vertebral bomb radiocarbon suggests extreme longevity in white sharks. PLoS One 9:e84006. doi: 10.1371/journal.pone.0084006 CrossRefGoogle Scholar
  35. Hussey NE, McCann H, Cliff G, Dudley SFJ, Wintner S, Fisk AT (2012) Size-based analysis of diet and trophic position of the white shark (Carcharodon carcharias) in South African waters. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 27–50. doi: 10.1201/b11532-5 CrossRefGoogle Scholar
  36. Huveneers C, Stead J, Bennett MB, Lee KA, Harcourt RG (2013) Age and growth determination of three sympatric wobbegong sharks: How reliable is growth band periodicity in Orectolobidae? Fish Res 147:413–425. doi: 10.1016/j.fishres.2013.03.014 CrossRefGoogle Scholar
  37. Kalish JM (1993) Pre- and post-bomb radiocarbon in fish otoliths. Earth Planet Sci Lett 114:549–554. doi: 10.1016/0012-821X(93)90082-K CrossRefGoogle Scholar
  38. 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, pp 637–653Google Scholar
  39. Kerr LA, Andrews AH, Cailliet GM, Brown TA, Coale KH (2006) Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environ Biol Fish 77:337–353. doi: 10.1007/s10641-006-9125-1 CrossRefGoogle Scholar
  40. Kneebone J, Natanson LJ, Andrews AL, Hunt Howell W (2008) Using bomb radiocarbon analyses to validate age and growth estimates for the tiger shark, Galeocerdo cuvier, in the western North Atlantic. Mar Biol 154:423–434. doi: 10.1007/s00227-008-0934-y CrossRefGoogle Scholar
  41. Lai HL, Gunderson DR (1987) Effects of ageing errors on estimates of growth mortality and yield per recruit for walleye, Pollock (Theragra chalcogramma). Fish Res 5:287–302CrossRefGoogle Scholar
  42. Natanson LJ, Cailliet GM (1990) Vertebral growth zone deposition in Pacific angle sharks. Copeia 4:1133–1145. doi: 10.2307/1446499 CrossRefGoogle Scholar
  43. Natanson LJ, Skomal GB (2015) Age and growth of the white shark, Carcharodon carcharias, in the western North Atlantic Ocean. Mar Freshw Res 66:387–398. doi: 10.1071/MF14127 CrossRefGoogle Scholar
  44. Natanson LJ, Mello JJ, Campana SE (2002) Validated age and growth of the porbeagle shark, Lamna nasus, in the western north Atlantic Ocean. Fish Bull 100:266–278Google Scholar
  45. Natanson LJ, Wintner SP, Johansson F et al (2008) Ontogenetic vertebral growth patterns in the basking shark Cetorhinus maximus. Mar Ecol Prog Ser 361:267–278. doi: 10.3354/meps07399 CrossRefGoogle Scholar
  46. Natanson LJ, Gervelis BJ, Winton MV, Hamady LL, Gulak SJB, Carlson JK (2014) Validated age and growth estimates for Carcharhinus obscurus in the northwestern Atlantic Ocean, with pre- and post management growth comparisons. Environ Biol Fish 97:881–896. doi: 10.1007/s10641-013-0189-4 CrossRefGoogle Scholar
  47. Natanson LJ, Hamady LL, Gervelis BJ (2015) Analysis of bomb radiocarbon data for common thresher sharks, Alopias vulpinus, in the northwestern Atlantic Ocean with revised growth curves. Environ Biol Fish 99:39–47. doi: 10.1007/s10641-015-0452-y CrossRefGoogle Scholar
  48. Passerotti MS, Carlson JK, Piercy AN, Campana SE (2010) Age validation of great hammerhead shark (Sphyrna Mokarran), determined by bomb radiocarbon analysis. Fish Bull 108:346–351Google Scholar
  49. Passerotti MS, Andrews AH, Carlson JK, Wintner SP, Goldman KJ, Natanson LJ (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. Mar Freshw Res 65:674–687. doi: 10.1071/MF13214 CrossRefGoogle Scholar
  50. Porter ME, Beltrán JL, Koob TJ, Summers AP (2006) Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondricthyes). J Exp Biol 209:2920–2928. doi: 10.1242/jeb.02325 CrossRefGoogle Scholar
  51. Pratt HL (1996) Reproduction in the male white shark. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 131–138. doi: 10.1016/B978-012415031-7/50014-8 CrossRefGoogle Scholar
  52. Ridewood WG (1921) On the calcification of the vertebral centra in sharks and rays. Phil Trans R Soc B 210:311–407. doi: 10.1098/rstb.1921.0008 CrossRefGoogle Scholar
  53. Roark EB, Guilderson TP, Dunbar RB, Ingram BL (2006) Radiocarbon based ages and growth rates: Hawaiian deep sea corals. Mar Ecol Prog Ser 327:1–14. doi: 10.3354/meps327001 CrossRefGoogle Scholar
  54. Schnute J (1981) A versatile growth model with statistically stable parameters. Can J Fish Aquat Sci 38:1128–1140CrossRefGoogle Scholar
  55. Smale M, Cliff G (2012) White sharks and cephalopod prey: indicators of habitat use? In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 51–57. doi: 10.1201/b11532-6 CrossRefGoogle Scholar
  56. Smith SE, Au DW, Show C (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Mar Freshw Res 49:663–678. doi: 10.1071/MF97135 CrossRefGoogle Scholar
  57. Stuiver M, Polach HA (1977) Discussion reporting of 14C data. Radiocarbon 19:355–363Google Scholar
  58. Tanaka S, Kitamura T, Mochizuki T, Kofuji K (2011) Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kahima-nada, Japan. Mar Freshw Res 62:548–556. doi: 10.1071/MF10130 CrossRefGoogle Scholar
  59. Towner AV, Wcisel MA, Reisinger RR, Edwards D, Jewell OJD (2013) Gauging the threat: the first population estimate for white sharks in South Africa using photo identification and automated software. PLoS One 8:e66035. doi: 10.1371/journal.pone.0066035 CrossRefGoogle Scholar
  60. Tricas TC, McCosker JE (1984) Predatory behavior of the white shark (Carcharodon carcharias), with notes on its biology. Pro Calif Acad Sci 43:221–238Google Scholar
  61. Uchida S, Toda M, Teshima K, Yano K (1996) Pregnant white sharks and full-term embryos from Japan. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 139–155. doi: 10.1016/B978-012415031-7/50015-X CrossRefGoogle Scholar
  62. Weidman CB, Jones GA (1993) A shell-derived time history of bomb 14C on Georges Bank and its Labrador Sea implications. J Geophys Res 98:14577–14588. doi: 10.1029/93JC00785 CrossRefGoogle Scholar
  63. Wintner SP, Cliff G (1999) Age and growth determination of the white shark, Carcharodon carcharias, from the east coast of South Africa. Fish Bull 97:153–169Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Heather M. Christiansen
    • 1
    Email author
  • Steven E. Campana
    • 2
    • 7
  • Aaron T. Fisk
    • 1
  • Geremy Cliff
    • 3
    • 4
  • Sabine P. Wintner
    • 3
    • 4
  • Sheldon F. J. Dudley
    • 5
  • Lisa A. Kerr
    • 6
  • Nigel E. Hussey
    • 1
  1. 1.Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada
  2. 2.Population Ecology DivisionBedford Institute of OceanographyDartmouthCanada
  3. 3.KwaZulu-Natal Sharks BoardUmhlanga RocksSouth Africa
  4. 4.Biomedical Resource UnitUniversity of KwaZulu-NatalDurbanSouth Africa
  5. 5.Department of AgricultureForestry and FisheriesRogge Bay, Cape TownSouth Africa
  6. 6.Gulf of Maine Research InstitutePortlandUSA
  7. 7.Life and Environmental SciencesUniversity of IcelandReykjavíkIceland

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