Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kashima-nada, Japan

S. Tanaka A D , T. Kitamura B , T. Mochizuki C and K. Kofuji C
+ Author Affiliations
- Author Affiliations

A School of Marine Science and Technology, Tokai University, 3-20-1 Orido, Shimizu, Shizuoka 424-8610, Japan.

B Environmental Science Laboratory, Japan NUS Co., 1-1 Fukuura, Kanazawa, Yokohama 236-0004, Japan.

C Ibaraki Prefectural Oarai Aquarium, 8252-3 Isohama-machi, Oarai, Higashi-Ibaraki 311-1301, Japan.

D Corresponding author. Email: sho@scc.u-tokai.ac.jp

Marine and Freshwater Research 62(6) 548-556 https://doi.org/10.1071/MF10130
Submitted: 8 June 2010  Accepted: 6 January 2011   Published: 24 June 2011

Journal Compilation © CSIRO Publishing 2011 Open Access CC BY-NC-ND

Abstract

The white shark, a top predator inhabiting the world’s oceans, is an endangered species. However, knowledge of its life-history traits and population structure is still limited. We hypothesised that life-history traits would vary among populations because the species’ various habitats are diverse and change through time. Age was estimated by counting growth bands in the centra of white sharks caught in Japan. The von Bertalanffy growth parameters were estimated at L = 455 cm TL, k = 0.196 year–1 and t0 = –1.92 years for males and L = 607 cm TL, k = 0.159 year–1 and t0 = –1.80 years for females. The growth rate to maturity was higher than that known for individuals from California and South Africa. Male sharks matured at 310 cm TL at 4 years of age and females began to mature at ~450 cm TL and 7 years. The D-loop-region sequences of mitochondrial DNA extracted from Japanese white sharks and GenBank datasets from sharks of California, Australia, New Zealand and South Africa indicate that Japanese white sharks form a monophyletic clade separate from the populations of other regions. The results suggest that unique life-history traits of Japanese white sharks may be caused by genetic differences.

Additional keywords: growth rate, maturity, corpus calcaeum, population, white shark.


References

Ainley, D. G., Henderson, R. P., Huber, H. R., Boekelheide, R. J., Allen, S. G., et al. (1985). Dynamics of white shark/pinniped interactions in the Gulf of the Farallones. Memoirs of the Southern California Academy of Sciences 9, 109–122.

Akamine, T. (2004). Statistical test and model selection of fish growth formula. Bulletin of the Japanese Society of Fisheries Oceanography 68, 44–51.

Bonfil, R., Meyer, M., Scholl, M. C., Johnson, R., O’Brien, S., et al. (2005). Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310, 100–103.
Transoceanic migration, spatial dynamics, and population linkages of white sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOjsr7N&md5=dbb22b5fbf790fa57faac3fa3dea5958CAS | 16210537PubMed |

Bonfil, R., Francis, M. P., Duffy, C., Manning, M. J., and O’Brien, S. (2010). Large-scale tropical movements and diving behavior of white sharks Carcharodon carcharias tagged off New Zealand. Aquatic Biology 8, 115–123.
Large-scale tropical movements and diving behavior of white sharks Carcharodon carcharias tagged off New Zealand.Crossref | GoogleScholarGoogle Scholar |

Boustany, A. M., Davis, S. F., Pyle, P., Anderson, S. D., Le Boeuf, B. J., et al. (2002). Expanded niche for white sharks. Nature 415, 35–36.
Expanded niche for white sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xkt1Kjtg%3D%3D&md5=0af179efad5edb659b342540d69b943cCAS |

Bruce, B. D., Stevens, J. D., and Malcolm, H. (2006). Movements and swimming behaviour of white sharks (Carcharodon carcharias) in Australian waters. Marine Biology 150, 161–172.
Movements and swimming behaviour of white sharks (Carcharodon carcharias) in Australian waters.Crossref | GoogleScholarGoogle Scholar |

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

Cailliet, G. M., and Radtke, R. L. (1987). A progress report on the electron microprobe analysis techniques for age determination and verification in elasmobranchs. In ‘The Age and Growth of Fish’. (Eds R. C. Summerfelt and G. E. Hall.) pp. 359–369. (The Iowa State University Press: Ames, IA.)

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. Memoirs of the Southern California Academy of Sciences 9, 49–60..

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 | GoogleScholarGoogle Scholar |

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

Cassoff, R. M., Campana, S. E., and Myklevoll, S. (2007). Changes in baseline growth and maturation parameters of northwest Atlantic porbeagle, Lamna nasus, following heavy exploitation. Canadian Journal of Fisheries and Aquatic Sciences 64, 19–29.
Changes in baseline growth and maturation parameters of northwest Atlantic porbeagle, Lamna nasus, following heavy exploitation.Crossref | GoogleScholarGoogle Scholar |

Cerna, F., and Licandeo, R. (2009). Age and growth of the shortfin mako (Isurus oxyrinchus) in the south-eastern Pacific off Chile. Marine and Freshwater Research 60, 394–403.
Age and growth of the shortfin mako (Isurus oxyrinchus) in the south-eastern Pacific off Chile.Crossref | GoogleScholarGoogle Scholar |

Cliff, G., Van Der Elst, R. P., Govender, A., Witthuhn, T. K., and Bullen, E. M. (1996). First estimate of mortality and population size of white sharks on the South African coast. In ‘Great White Sharks: The Biology of Carcharodon carcharias’. (Eds A. P. Klimley and D. G. Ainley.) pp. 393–400. (Academic Press: Millbrae, CA.)

Dewar, H., Domeier, M., and Nasby-Lucas, N. (2004). Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight. Environmental Biology of Fishes 70, 133–143.
Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight.Crossref | GoogleScholarGoogle Scholar |

Domeier, M. L., and Nasby-Lucas, N. (2008). Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging area. Marine Ecology Progress Series 370, 221–237.
Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging area.Crossref | GoogleScholarGoogle Scholar |

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |

Francis, R. I. C. C. (1990). Back-calculation of fish length: a critical review. Journal of Fish Biology 36, 883–902.
Back-calculation of fish length: a critical review.Crossref | GoogleScholarGoogle Scholar |

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: Millbrae, CA.)

Francis, M. P., Campana, S. E., and Jones, C. M. (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? Marine and Freshwater Research 58, 10–23.
Age under-estimation in New Zealand porbeagle sharks (Lamna nasus): is there an upper limit to ages that can be determined from shark vertebrae?Crossref | GoogleScholarGoogle Scholar |

Gubili, C., Johnson, R., Gennari, E., Oosthuizen, W. H., Kotze, D., et al. (2009). Concordance of genetic and fin photo identification in the great white shark, Carcharodon carcharias, off Mossel Bay, South Africa. Marine Biology 156, 2199–2207.
Concordance of genetic and fin photo identification in the great white shark, Carcharodon carcharias, off Mossel Bay, South Africa.Crossref | GoogleScholarGoogle Scholar |

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |

Huelsenbeck, J. P., and Ronquist, F. (2001). ‘MRBAYES: Bayesian Inference of Phylogenic Trees.’ (Oxford University Press: New York.)

Jorgensen, C., Enberg, K., Dunlop, E. S., Arlinghaus, R., Boukal, D. S., et al. (2007). Managing evolving fish stocks. Science 318, 1247–1248.
Managing evolving fish stocks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOmsbfF&md5=7a484a2248ef33b0a4c0c2c94181626cCAS | 18033868PubMed |

Jorgensen, S. J., Reeb, C. A., Chapple, T. K., Anderson, S., Perle, C., et al. (2010). Philopatry and migration of Pacific white sharks. Proceedings of the Royal Society B: Biological Sciences 277, 679–688.
Philopatry and migration of Pacific white sharks.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=b624e05c6d4a1dff9a13279cf8cb9101CAS | 7463489PubMed |

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 | GoogleScholarGoogle Scholar |

Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=eaed9e037de7ef0b04ef944fbe4e51e5CAS | 15260895PubMed |

Magnussen, E. (2007). Interpopulation comparison of growth patterns of 14 fish species on Faroe Bank: are all fishes on the bank fast-growing? Journal of Fish Biology 71, 453–475.
Interpopulation comparison of growth patterns of 14 fish species on Faroe Bank: are all fishes on the bank fast-growing?Crossref | GoogleScholarGoogle Scholar |

Mollet, H. F., Cailliet, G. M., Klimley, A. P., Ebert, D. A., Testi, A. D., et al. (1996). A review of length validation methods and protocols to measure large white sharks. In ‘Great White Sharks: The Biology of Carcharodon carcharias’. (Eds A. P. Klimley and D. G. Ainley.) pp. 91–108. (Academic Press: Millbrae, CA.)

Nakaya, K. (1993). A fatal attack by a white shark in Japan and a review of shark attcks in Japanese waters. Japanese Journal of Ichthyology 40, 35–42..

Nakaya, K. (1994). Distribution of white shark in Japanese waters. Fisheries Science 60, 515–518..
| 1:CAS:528:DyaK2MXitFeku7s%3D&md5=94dff0e275a6d12d83bace39f8880dbdCAS |

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..

Natanson, L. J., Wintner, S. P., Johansson, F., Piercy, A., Campbell, P., et al. (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 | GoogleScholarGoogle Scholar |

Nylander, J. A. A. (2004). MrAIC.pl. Program distributed by the author, Evolutionary Biology Centre, Uppsala University, Sweden. Available athttp://www.abc.se/~nylander/mraic/mraic.html [Accessed 19 November 2010].

Okamura, H., and Semba, Y. (2009). A novel statistical method for validating the periodicity of vertebral growth band formation in elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 66, 771–780.
A novel statistical method for validating the periodicity of vertebral growth band formation in elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |

Pardini, A. T., Jones, C. S., Scholl, M. C., and Noble, L. R. (2000). Isolation and characterization of dinucleotide microsatellite loci in the great white shark, Carcharodon carcharias. Molecular Ecology 9, 1176–1178.
Isolation and characterization of dinucleotide microsatellite loci in the great white shark, Carcharodon carcharias.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVWgsrs%3D&md5=ec48aa4c0dde272fef3606579c8c9e28CAS | 10964240PubMed |

Pardini, A. T., Jones, C. S., Noble, L. R., Kreiser, B., Malcolm, H., et al. (2001). Sex-biased dispersal of great white sharks. Nature 412, 139–140.
Sex-biased dispersal of great white sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFWnsr4%3D&md5=3bcf499d9706ee72315bc42cd06bd219CAS | 11449258PubMed |

Pratt, H. L., Jr (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: Millbrae, CA.)

Ridewood, W. G. (1921). On the calcification of the vertebral centra in sharks and rays. Phylosophical Transactions of Royal Society London series B 210, 311–407.
On the calcification of the vertebral centra in sharks and rays.Crossref | GoogleScholarGoogle Scholar |

Robbins, R. L. (2007). Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia. Journal of Fish Biology 70, 1350–1364.
Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia.Crossref | GoogleScholarGoogle Scholar |

Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425..
| 1:STN:280:DyaL1c7ovFSjsA%3D%3D&md5=7797e863e348f56c62d0bd24725b6873CAS | 3447015PubMed |

Semba, Y., Nakano, H., and Aoki, I. (2009). Age and growth analysis of the shortfin mako, Isurus oxyrinchus, in the western and central North Pacific Ocean. Environmental Biology of Fishes 84, 377–391.
Age and growth analysis of the shortfin mako, Isurus oxyrinchus, in the western and central North Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Shimamoto, N., Tanda, M., Nakamura, Y., Otani, T., Nishikawa, T., et al. (1994). Record of the white shark Carcharodon carcharias caught in Sea of Harima in May 1992. Bulletin of the Hyogo Prefectural Fisheries Experimental Station 31, 79–84..

Smith, S. E., Mitchell, R. A., and Fuller, D. (2003). Age-validation of a leopard shark (Triakis semifasciata) recaptured after 20 years. Fishery Bulletin 101, 194–198..

Strong, W. R., Jr, Bruce, B. D., Nelson, D. R., and Murphy, R. D. (1996). Population dynamics of white sharks in Spencer Gulf, South Australia. In ‘Great White Sharks: The Biology of Carcharodon carcharias’. (Eds A. P. Klimley and D. G. Ainley.) pp. 401–414. (Academic Press: Millbrae, CA.)

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. 139–155. (Academic Press: Millbrae, CA.)

Weng, K. C., Boustany, A. M., Pyle, P., Anderson, S. D., Brown, A., et al. (2007). Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Marine Biology 152, 877–894.
Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Weng, K. C., O’Sullivan, J. B., Lowe, C. G., Winkler, C. E., Dewar, H., et al. (2007). Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific. Marine Ecology Progress Series 338, 211–224.
Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific.Crossref | GoogleScholarGoogle Scholar |

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..

Zenger, K. R., Stow, A. J., Peddemors, V., Briscoe, D. A., and Harcourt, R. G. (2006). Widespread utility of highly informative AFLP molecular markers across divergent shark species. The Journal of Heredity 97, 607–611.
Widespread utility of highly informative AFLP molecular markers across divergent shark species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCru7nI&md5=34d342d98d055348c6424c02596fbd21CAS | 17150982PubMed |