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Advances in the aquatic sciences
RESEARCH ARTICLE

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

M. S. Passerotti A F , A. H. Andrews B , J. K. Carlson A , S. P. Wintner C , K. J. Goldman D and L. J. Natanson E
+ Author Affiliations
- Author Affiliations

A National Marine Fisheries Service, Southeast Fisheries Science Center, 3500 Delwood Beach Road, Panama City, FL 32408, USA.

B National Marine Fisheries Service, Pacific Islands Fisheries Science Center, 99-193 Aiea Heights Drive #417, Aiea, HI 96701, USA.

C KwaZulu-Natal Sharks Board and Biomedical Resource Unit, University of KwaZulu-Natal, Durban 4056, South Africa.

D Alaska Department of Fish and Game, Division of Commercial Fisheries, 3298 Douglas Place, Homer, AK 99603, USA.

E National Marine Fisheries Service, Apex Predators Program, 28 Tarzwell Drive, Narragansett, RI 02882, USA.

F Corresponding author. Email: mpasserotti@gmail.com

Marine and Freshwater Research 65(8) 674-687 https://doi.org/10.1071/MF13214
Submitted: 9 August 2013  Accepted: 8 October 2013   Published: 29 January 2014

Abstract

Bomb radiocarbon analysis of vertebral growth bands was used to validate lifespan for sand tiger sharks (Carcharias taurus) from the western North Atlantic (WNA) and southwestern Indian Oceans (SIO). Visual counts of vertebral growth bands were used to assign age and estimate year of formation (YOF) for sampled growth bands in eight sharks from the WNA and two sharks from the SIO. Carbon-14 results were plotted relative to YOF for comparison with regional Δ14C reference chronologies to assess the accuracy of age estimates. Results from the WNA validated vertebral age estimates up to 12 years, but indicated that ages of large adult sharks were underestimated by 11–12 years. Age was also underestimated for adult sharks from the SIO by 14–18 years. Validated lifespan for C. taurus individuals in the present study reached at least 40 years for females and 34 years for males. Findings indicated that the current age-reading methodology is not suitable for estimating the age of C. taurus beyond ~12 years. Future work should investigate whether vertebrae of C. taurus record age throughout ontogeny, or cease to be a reliable indicator at some point in time.

Additional keywords: carbon-14, longevity, ragged tooth shark, spikkel-skeurtandhaai.


References

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.

Ardizzone, D., Cailliet, G. M., Natanson, L. J., Andrews, A. H., 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 |

Bansemer, C. S., and Bennett, M. B. (2009). Reproductive periodicity, localized movements and behavioural segregation of pregnant Carcharias taurus at Wolf Rock, southeast Queensland, Australia. Marine Ecology Progress Series 374, 215–227.
Reproductive periodicity, localized movements and behavioural segregation of pregnant Carcharias taurus at Wolf Rock, southeast Queensland, Australia.CrossRef |

Bard, E., Arnold, M., Toggweiler, J. R., Maurice, P., and Duplessy, J. C. (1989). Bomb 14C in the Indian Ocean measured by accelerator mass spectrometry: oceanographic implications. Radiocarbon 31, 510–522.

Branstetter, S., and Musick, J. A. (1994). Age and growth estimates for the sand tiger shark in the Northwestern Atlantic Ocean. Transactions of the American Fisheries Society 123, 242–254.
Age and growth estimates for the sand tiger shark in the Northwestern Atlantic Ocean.CrossRef |

Broecker, W. S., and Peng, T.-H. (1982). ‘Tracers in the Sea.’ (Lamont-Doherty Geological Observatory: Palisades, New York.)

Cailliet, G. M., Smith, W. D., Mollet, H. F., and Goldman, K. J. (2006). Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting. Environmental Biology of Fishes 77, 211–228.
Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting.CrossRef |

Campana, S. E. (2001). Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology 59, 197–242.
Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods.CrossRef |

Campana, S. E., and Jones, C. M. (1998). Radiocarbon from nuclear testing applied to age validation of black drum, Pogonias cromis. Fishery Bulletin 96, 185–192.

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

Campana, S. E., Jones, C., McFarlane, G. A., and Myklevoll, S. (2006). Bomb dating and age validation using the spines of spiny dogfish (Squalus acanthias). Environmental Biology of Fishes 77, 327–336.
Bomb dating and age validation using the spines of spiny dogfish (Squalus acanthias).CrossRef |

Campana, S. E., Casselman, J. M., and Jones, C. M. (2008). Bomb radiocarbon chronologies in the Arctic, with implications for the age validation of lake trout (Salvelinus namaycush) and other Arctic species. Canadian Journal of Fisheries and Aquatic Sciences 65, 733–743.
Bomb radiocarbon chronologies in the Arctic, with implications for the age validation of lake trout (Salvelinus namaycush) and other Arctic species.CrossRef |

Carlson, J. K., McCandless, C. T., Cortés, E., Grubbs, R. D., Andrews, K. I., MacNeil, M. A., and Musick, J. A. (2009). An update on the status of the sand tiger shark, Carcharias taurus, in the Northwest Atlantic Ocean. National Oceanic Atmospheric Administration Technical Memorandum NMFS–SEFSC-585. Silver Spring, MD.

Chidlow, J. A., Simpfendorfer, C. A., and Russ, G. R. (2007). Variable growth band deposition leads to age and growth uncertainty in the western wobbegong shark, Orectolobus hutchinsi. Marine and Freshwater Research 58, 856–865.
Variable growth band deposition leads to age and growth uncertainty in the western wobbegong shark, Orectolobus hutchinsi.CrossRef |

Chin, A., Simpfendorfer, C., Tobin, A., and Heupel, M. (2013). Validated age, growth and reproductive biology of Cacharhinus melanopterus, a widely distributed and exploited reef shark. Marine and Freshwater Research 64, 965–975.
Validated age, growth and reproductive biology of Cacharhinus melanopterus, a widely distributed and exploited reef shark.CrossRef |

Cliff, G. (1989). The breeding migration of the sand tiger shark, Carcharias taurus, in southern African waters. In ‘Abstracts of the 5th Annual Meeting of the American Elasmobranch Society, San Francisco, June 1989’. p. 76. San Francisco State University and California Academy of Science, San Francisco, CA.

Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 1: Hexanchiformes to Lamniformes. FAO Fisheries Synopsis 125, 1–249.

Dicken, M. L., Smale, M. J., and Booth, A. J. (2006). Spatial and seasonal distribution patterns of the ragged-tooth shark Carcharias taurus along the coast of South Africa. African Journal of Marine Science 28, 603–616.
Spatial and seasonal distribution patterns of the ragged-tooth shark Carcharias taurus along the coast of South Africa.CrossRef |

Dicken, M. L., Booth, A. J., Smale, M. J., and Cliff, G. (2007). Spatial and seasonal distribution patterns of juvenile and adult raggedtooth sharks (Carcharias taurus) tagged off the east coast of South Africa. Marine and Freshwater Research 58, 127–134.
Spatial and seasonal distribution patterns of juvenile and adult raggedtooth sharks (Carcharias taurus) tagged off the east coast of South Africa.CrossRef |

Druffel, E. R. M. (1989). Decade time scale variability of ventilation in the north Atlantic: high precision measurements of bomb radiocarbon in banded corals. Journal of Geophysical Research 94, 3271–3285.
Decade time scale variability of ventilation in the north Atlantic: high precision measurements of bomb radiocarbon in banded corals.CrossRef | 1:CAS:528:DyaL1MXmtFyqsL0%3D&md5=fa3c902783b4448bf61158430a471e67CAS |

Druffel, E. R. M. (2002). Radiocarbon in corals: records of the carbon cycle, surface circulation and climate. Oceanography 15, 122–127.
Radiocarbon in corals: records of the carbon cycle, surface circulation and climate.CrossRef |

Druffel, E. R. M., and Linick, T. W. (1978). Radiocarbon in annual coral rings of Florida. Geophysical Research Letters 5, 913–916.
Radiocarbon in annual coral rings of Florida.CrossRef | 1:CAS:528:DyaE1MXktFKgug%3D%3D&md5=f474598ab12c33952dff91b9f5e4591cCAS |

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 |

Fry, B. (1988). Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnology and Oceanography 33, 1182–1190.
Food web structure on Georges Bank from stable C, N, and S isotopic compositions.CrossRef | 1:CAS:528:DyaL1MXksVCktg%3D%3D&md5=7a192e395420cfd1bc703c460dc748efCAS |

Gelsleichter, J., Musick, J. A., and Nichols, S. (1999). Food habits of the smooth dogfish, Mustelus canis, dusky shark, Carcharhinus obscurus, Atlantic sharpnose shark, Rhizoprionodon terraenovae, and the sand tiger, Carcharias taurus, from the northwest Atlantic Ocean. Environmental Biology of Fishes 54, 205–217.
Food habits of the smooth dogfish, Mustelus canis, dusky shark, Carcharhinus obscurus, Atlantic sharpnose shark, Rhizoprionodon terraenovae, and the sand tiger, Carcharias taurus, from the northwest Atlantic Ocean.CrossRef |

Gilmore, R. G. (1993). Reproductive biology of lamnoid sharks. Environmental Biology of Fishes 38, 95–114.
Reproductive biology of lamnoid sharks.CrossRef |

Gilmore, R. G., Dodrill, J. W., and Linley, P. A. (1983). Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). Fishery Bulletin 81, 201–225.

Gilmore, R. G., Putz, O., and Dodrill, J. W. (2005). Oophagy, intrauterine cannibalism and reproductive strategy in lamnoid sharks. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras’. (Ed W. C. Hamlett.) pp. 435–462. (Science Publishers: Enfield, NH.)

Goldman, K. J. (2002). Aspects of age, growth, demographics and thermal biology of two lamniform shark species. Ph.D. Dissertation, School of Marine Science, College of William and Mary, Virginia Institute of Marine Science, Goucester Point, VA.

Goldman, K. J., Branstetter, S. E., and Musick, J. A. (2006). A re-examination of the age and growth of sand tiger sharks, Carcharias taurus, in the western North Atlantic: the importance of ageing protocols and use of multiple back-calculation techniques. Environmental Biology of Fishes 77, 241–252.
A re-examination of the age and growth of sand tiger sharks, Carcharias taurus, in the western North Atlantic: the importance of ageing protocols and use of multiple back-calculation techniques.CrossRef |

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.)

Gordon, A. L. (1986). Interocean exchange of thermocline water. Journal of Geophysical Research 91, 5037–5046.
Interocean exchange of thermocline water.CrossRef |

Grottoli, A. G., and Eakin, C. M. (2007). A review of modern coral δ18O and Δ14C proxy records. Earth-Science Reviews 81, 67–91.
A review of modern coral δ18O and Δ14C proxy records.CrossRef |

Grumet, N. S., Guilderson, T. P., and Dunbar, R. B. (2002). Meridional transport in the Indian Ocean traced by coral radiocarbon. Journal of Marine Research 60, 725–742.
Meridional transport in the Indian Ocean traced by coral radiocarbon.CrossRef | 1:CAS:528:DC%2BD3sXit1emurc%3D&md5=d866319eb2c78278fb7ba38b2ffd800cCAS |

Henningsen, A. D., Smale, M. J., Gordon, I., Garner, R., Marin-Osorno, R., and Kinnunen, N. (2004). Captive breeding and sexual conflict in elasmobranchs. In ‘The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives.’ (Eds M. Smith, D. Warmolts, D. Thorney and R. Heuter.) pp. 237–248. (Ohio Biological Survey: Columbus, OH.)

Hutchins, B., and Thompson, M. (1983). ‘The Marine and Estuarine Fishes of South Western Australia.’ (Western Australian Museum: Perth.)

Huveneers, C., Stead, J., Bennett, M. B., Lee, K. A., and Harcourt, R. G. (2013). Age and growth determination of three sympatric wobbegong sharks: how reliable is growth band periodicity in Orectolobidae? Fisheries Research , .
Age and growth determination of three sympatric wobbegong sharks: how reliable is growth band periodicity in Orectolobidae?CrossRef |

Kalish, J. M. (2001). Use of the bomb radiocarbon chronometer to validate fish age. Final Report FRDC Project 93/109. Fisheries Research and Development Corporation, Canberra.

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, FRDC Project 93/109.’ (Ed J. M. Kalish.) pp. 116–122. Fisheries Research and Development Corporation, Canberra.

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

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 |

Kneebone, J., Chisholm, J., and Skomal, G. B. (2012). Seasonal residency, habitat use, and site fidelity of juvenile sand tiger sharks Carcharias taurus in a Massachusetts estuary. Marine Ecology Progress Series 471, 165–181.
Seasonal residency, habitat use, and site fidelity of juvenile sand tiger sharks Carcharias taurus in a Massachusetts estuary.CrossRef |

Kohler, N. E., Casey, J. G., and Turner, P. A. (1998). NMFS cooperative shark tagging program, 1962–1993: an atlas of shark tag and recapture data. Marine Fisheries Review 60, 1–87.

Last, P. R., and Stevens, J. D. (1994). ‘Sharks and Rays of Australia.’ (CSIRO: Melbourne.)

Lucifora, L. (2003). Ecología y conservación de los grandes tiburones costeros de Bahía Anegada, provincia de Buenos Aires, Argentina. Ph.D. Dissertation, Universidad Nacional, Facultad de Ciencias Exactas y Naturales, Mar del Plata, Argentina.

Lutjeharms, J. R. E., Cooper, J., and Roberts, M. (2000). Upwelling at the inshore edge of the Agulhas Current. Continental Shelf Research 20, 737–761.
Upwelling at the inshore edge of the Agulhas Current.CrossRef |

Musick, J. A. (1999). Criteria to define extinction risk in marine fishes. Fisheries 24, 6–14.
Criteria to define extinction risk in marine fishes.CrossRef |

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 |

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., Hemida, F., Mollen, F. H., Vanni, S., Burgess, G. H., Compagno, L. J. V., and Wedderburn-Maxwell, A. (2008). Ontogenetic vertebral growth patterns in the basking shark Cetorhinus maximus. Marine Ecology Progress Series 361, 267–278.
Ontogenetic vertebral growth patterns in the basking shark Cetorhinus maximus.CrossRef |

National Marine Fisheries Service (NMFS) (2009). Final amendment 1 to the 2006 Consolidated Atlantic highly migratory species fishery management plan. Essential fish habitat. National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Office of Sustainable Fisheries, Highly Migratory Species Management Division, Silver Spring, MD.

Olsson, I. U. (1970). The use of oxalic acid as a standard. In ‘Radiocarbon Variations and Absolute Chronology. Proceedings of the 12th Nobel Symposium.’ (Ed. I. U. Olsson.) p. 17. (John Wiley & Sons: New York.)

Otway, N. M., and Ellis, M. T. (2011). Pop-up archival satellite tagging of Carcharias taurus movements and depth/temperature-related use of south-eastern Australian waters. Marine and Freshwater Research 62, 607–620.
Pop-up archival satellite tagging of Carcharias taurus movements and depth/temperature-related use of south-eastern Australian waters.CrossRef | 1:CAS:528:DC%2BC3MXnvFanu7s%3D&md5=da32a9e4cd02220e0561790fae02f82fCAS |

Passerotti, M. S., Carlson, J. K., Piercy, A. N., and Campana, S. E. (2010). Age validation of great hammerhead shark (Sphyrna mokarran), determined by bomb radiocarbon analysis. Fishery Bulletin 108, 346–351.

Pollard, D., and Smith, A. (2009). Carcharias taurus. IUCN 2012: IUCN Red List of Threatened Species. (Version 2012.2). Available at http://www.iucnredlist.org [accessed 11 June 2013].

Pollard, D. A., Lincoln Smith, M. P., and Smith, A. K. (1996). The biology and conservation status of the grey nurse shark (Carcharias taurus Rafinesque 1810) in New South Wales, Australia. Aquatic Conservation: Marine and Freshwater Ecosystems 6, 1–20.
The biology and conservation status of the grey nurse shark (Carcharias taurus Rafinesque 1810) in New South Wales, Australia.CrossRef |

Reimer, P. J., Brown, T. A., and Reimer, R. W. (2004). Discussion: reporting and calibration of post-bomb 14C data. Radiocarbon 46, 1299–1304.
| 1:CAS:528:DC%2BD2MXpsVams7k%3D&md5=c3cab0c136ee907d93abb44c5d11f573CAS |

Smale, M. J. (2005). The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the Eastern Cape, South Africa. African Journal of Marine Science 27, 331–335.
The diet of the ragged-tooth shark Carcharias taurus Rafinesque 1810 in the Eastern Cape, South Africa.CrossRef |

Springer, S. (1939). Notes on the sharks of Florida. Proceedings of the Florida Academy of Science 3, 9–41.

Stuiver, M., and Polach, H. A. (1977). Reporting of C-14 data. Radiocarbon 19, 355–363.

Tanaka, S. (1990). Age and growth studies on the calcified structures of newborn sharks in laboratory aquaria using tetracycline. In ‘Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of Fisheries.’ (Eds H. L. Pratt Jr, S. H. Gruber and T. Taniuchi.) pp. 189–202. NOAA Technical Report 90, US Department of Commerce, National Marine Fisheries Service, Silver Spring, MD, USA.



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