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Advances in the aquatic sciences
RESEARCH ARTICLE

Positional and ontogenetic variation in vertebral centra morphology in five batoid species

Kelsey C. James https://orcid.org/0000-0002-9906-4789 A C D and Lisa J. Natanson B
+ Author Affiliations
- Author Affiliations

A Department of Fisheries, Animal and Veterinary Sciences, University of Rhode Island, 9 East Alumni Avenue, Kingston, RI 02881, USA.

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

C Present address: NOAA Fisheries, 8901 La Jolla Shores Drive, La Jolla, CA 92037, USA.

D Corresponding author. Email: kelsey.james@noaa.gov

Marine and Freshwater Research 72(6) 887-898 https://doi.org/10.1071/MF20183
Submitted: 7 June 2020  Accepted: 26 October 2020   Published: 24 December 2020

Abstract

An increasing number of studies on elasmobranchs have shown that band-pair counts in vertebral centra do not accurately reflect age. Research in sharks has indicated that the number of band pairs vary with body size and that centrum morphology is related to structural needs. A study of this kind has not been undertaken on batoids; thus, we examined the relationship between band-pair deposition and morphology of centra along the vertebral column, and ontogenetically, for five batoid species (little skate, Leucoraja erinacea, winter skate, Leucoraja ocellata, barndoor skate, Dipturus laevis, Atlantic stingray, Dasyatis sabina, and round ray, Urobatis halleri). Centrum morphology and band-pair count varied along the vertebral column in all individuals of all species, except in young of the year. Variation in band-pair counts among centra within individuals supports the hypothesis that band-pair formation is related to somatic growth and body shape rather than to an annual cycle.

Keywords: age, band-pair counts, skates and rays, somatic growth.


References

Beamish, R. J., and McFarlane, G. A. (1983). The forgotten requirement for age validation in fisheries biology. Transactions of the American Fisheries Society 112, 735–743.
The forgotten requirement for age validation in fisheries biology.Crossref | GoogleScholarGoogle Scholar |

Brown, C. A., and Gruber, S. H. (1988). Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra. Copeia 1988, 747–753.
Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra.Crossref | GoogleScholarGoogle Scholar |

Cailliet, G. M., and Goldman, K. J. (2004). Chapter 14. 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 LLC: Boca Raton, FL, USA.).

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., 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 | GoogleScholarGoogle Scholar |

Chang, W. Y. B. (1982). A statistical method for evaluating the reproducibility of age determination. Canadian Journal of Fisheries and Aquatic Sciences 39, 1208–1210.
A statistical method for evaluating the reproducibility of age determination.Crossref | GoogleScholarGoogle Scholar |

Clement, J. G. (1992). Re-examination of the fine structure of endoskeletal mineralization in chondrichthyans: implications for growth, ageing and calcium homeostasis. Australian Journal of Marine and Freshwater Research 43, 157–181.
Re-examination of the fine structure of endoskeletal mineralization in chondrichthyans: implications for growth, ageing and calcium homeostasis.Crossref | GoogleScholarGoogle Scholar |

Ebert, D. A. (2005). Reproductive biology of skates, Bathyraja (Ishiyama), along the eastern Bering Sea continental slope. Journal of Fish Biology 66, 618–649.
Reproductive biology of skates, Bathyraja (Ishiyama), along the eastern Bering Sea continental slope.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Fjelldal, P. G., Nordgarde, U., Berg, A., Grotmol, S., Totland, G. K., Wargelius, A., and Hansen, T. (2005). Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts. Aquaculture 250, 516–524.
Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts.Crossref | GoogleScholarGoogle Scholar |

Francis, M. P. (2006). Morphometric minefields: towards a measurement standard for chondrichthyan fishes. Environmental Biology of Fishes 77, 407–421.
Morphometric minefields: towards a measurement standard for chondrichthyan fishes.Crossref | GoogleScholarGoogle Scholar |

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 |

Gedamke, T. (2006). Developing a stock assessment for the barndoor skate (Dipturus laevis) in the Northeast United States. Ph.D. Dissertation, College of William and Mary, Virginia Institute of Marine Science, Williamsburg VA, USA. Dissertations, Theses, and Masters Projects. Paper 1539616663.

Haddon, M. (2001). ‘Modeling and Quantitative Measures in Fisheries.’ (Chapman & Hall/CRC Press: Boca Raton, FL, USA.)

Harry, A. V. (2018). Evidence of systemic age underestimation in shark and ray ageing studies. Fish and Fisheries 19, 185–200.
Evidence of systemic age underestimation in shark and ray ageing studies.Crossref | GoogleScholarGoogle Scholar |

Haskell, W. L. (1948). An investigation of the possibility of determining the age of sharks through annuli as shown in cross-sections of vertebrae. Annual Report of the Marine Laboratory of the Texas Game, and Fish Commission FY 1948–49, 212–217.

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 147, 413–425.
Age and growth determination of three sympatric wobbegong sharks: how reliable is growth band periodicity in Orectolobidae?Crossref | GoogleScholarGoogle Scholar |

Ingle, D. I., Natanson, L. J., and Porter, M. E. (2018). Mechanical behavior of shark vertebral centra at biologically relevant strains. The Journal of Experimental Biology 221, jeb188318.
Mechanical behavior of shark vertebral centra at biologically relevant strains.Crossref | GoogleScholarGoogle Scholar | 30352822PubMed |

Ishiyama, R. (1951). Studies on the rays and skates belonging to the family Rajidae, found in Japan and adjacent regions. 2. On the age-determination of Japanese black-skate Raja fusca. Nippon Suisan Gakkaishi 16, 112–118.
Studies on the rays and skates belonging to the family Rajidae, found in Japan and adjacent regions. 2. On the age-determination of Japanese black-skate Raja fusca.Crossref | GoogleScholarGoogle Scholar |

James, K. C. (2018). Analysis of band pair formation in elasmobranch vertebrae with implications for fisheries management. Ph.D. Dissertation, University of Rhode Island, Kingston RI, USA. Open Access Dissertations. Paper 760.

James, K. C. (2020). Vertebral growth and band-pair deposition in sexually mature little skates Leucoraja erinacea: is adult band-pair deposition annual? Journal of Fish Biology 96, 4–13.
Vertebral growth and band-pair deposition in sexually mature little skates Leucoraja erinacea: is adult band-pair deposition annual?Crossref | GoogleScholarGoogle Scholar | 31568576PubMed |

Jones, B. C., and Geen, G. H. (1977). Age determination of an elasmobranch (Squalus acanthias) by X-ray spectrometry. Journal of the Fisheries Research Board of Canada 34, 44–48.
Age determination of an elasmobranch (Squalus acanthias) by X-ray spectrometry.Crossref | GoogleScholarGoogle Scholar |

Kemp, N. E., and Westrin, S. K. (1979). Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. Journal of Morphology 160, 75–101.
Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks.Crossref | GoogleScholarGoogle Scholar | 458857PubMed |

McDowall, R. M. (1994). On size and growth in freshwater fish. Ecology Freshwater Fish 3, 67–79.
On size and growth in freshwater fish.Crossref | GoogleScholarGoogle Scholar |

McPhie, R. P., and Campana, S. E. (2009). Bomb dating and age determination of skates (family Rajidae) off the eastern coast of Canada. ICES Journal of Marine Science 66, 546–560.
Bomb dating and age determination of skates (family Rajidae) off the eastern coast of Canada.Crossref | GoogleScholarGoogle Scholar |

Natanson, L. J. (1993). Effect of temperature on band deposition in the little skate, Raja erinacea. Copeia 1993, 199–206.
Effect of temperature on band deposition in the little skate, Raja erinacea.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Natanson, L., Kohler, N., Ardizzone, D., Cailliet, G., Wintner, S., and Mollet, S. (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 | GoogleScholarGoogle Scholar |

Natanson, L. J., Sulikowski, J. A., Kneebone, J. R., and Tsang, P. C. (2007). Age and growth estimates for the smooth skate, Malacoraja senta, in the Gulf of Maine. Environmental Biology of Fishes 80, 293–308.
Age and growth estimates for the smooth skate, Malacoraja senta, in the Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |

Natanson, L. J., Wintner, S., Johansson, F., Piercy, A. N., Campbell, P., De Maddalena, A., Gulak, S. J., Human, B., Fulgosi, F. C., 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 | GoogleScholarGoogle Scholar |

Natanson, L. J., Skomal, G. B., Hoffmann, S., Porter, M., Goldman, K. J., and Serra, D. (2018). Age and growth of elasmobranchs: do band pairs on vertebral centra record age? Marine and Freshwater Research 69, 1440–1452.
Age and growth of elasmobranchs: do band pairs on vertebral centra record age?Crossref | GoogleScholarGoogle Scholar |

Officer, R. A., Gason, A. S., Walker, T. I., and Clement, J. G. (1996). Sources of variation in counts of growth increments in vertebrae from gummy shark, Mustelus antarcticus, and school shark, Galeorhinus galeus: implications for age determination. Canadian Journal of Fisheries and Aquatic Sciences 53, 1765–1777.
Sources of variation in counts of growth increments in vertebrae from gummy shark, Mustelus antarcticus, and school shark, Galeorhinus galeus: implications for age determination.Crossref | GoogleScholarGoogle Scholar |

Pierce, S. J., and Bennett, M. B. (2009). Validated annual band-pair periodicity and growth parameters of blue-spotted maskray Neotrygon kuhlii from south-east Queensland, Australia. Journal of Fish Biology 75, 2490–2508.
Validated annual band-pair periodicity and growth parameters of blue-spotted maskray Neotrygon kuhlii from south-east Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 20738504PubMed |

Piercy, A. N., Ford, T. S., Levy, L. M., and Snelson, F. F. (2006). Analysis of variability in vertebral morphology and growth ring counts in two carcharhinid sharks. Environmental Biology of Fishes 77, 401–406.
Analysis of variability in vertebral morphology and growth ring counts in two carcharhinid sharks.Crossref | GoogleScholarGoogle Scholar |

Porter, M. E., Beltran, J. L., Koob, T. J., and Summers, A. P. (2006). Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes). The Journal of Experimental Biology 209, 2920–2928.
Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes).Crossref | GoogleScholarGoogle Scholar | 16857876PubMed |

Porter, M. E., Koob, T. J., and Summers, A. P. (2007). The contribution of mineral to the material properties of vertebral cartilage from the smooth-hound shark Mustelus californicus. The Journal of Experimental Biology 210, 3319–3327.
The contribution of mineral to the material properties of vertebral cartilage from the smooth-hound shark Mustelus californicus.Crossref | GoogleScholarGoogle Scholar | 17872985PubMed |

R Core Team (2017). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/. [Accessed 20 May 2020]

Ridewood, W. G. (1921). On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 210, 311–407.

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, S. H. Gruber, and T. Taniuchi) NOAA technical report 90 (U.S. Department of Commerce), pp. 189–202.

Thomson, K. S., and Simanek, D. E. (1977). Body form and locomotion in sharks. American Zoologist 17, 343–354.
Body form and locomotion in sharks.Crossref | GoogleScholarGoogle Scholar |

Wilga, C. A. D., and Lauder, G. V. (2004). Chapter 5. Biomechanics of locomotion in sharks, rays, and chimeras. In ‘Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 139–164. (CRC Press LLC: Boca Raton, FL, USA.)

Wood, S. N. (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society. Series B. Methodological 73, 3–36.
Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models.Crossref | GoogleScholarGoogle Scholar |