Preliminary age and growth of the deep-water goblin shark Mitsukurina owstoni (Jordan, 1898)
Fabio P. Caltabellotta
A B F , Zachary A. Siders B , Gregor M. Cailliet C , Fabio S. Motta D and Otto B. F. Gadig E
+ Author Affiliations
- Author Affiliations
A Coastal Oregon Marine Experiment Station, Oregon State University, 2030 SE Marine Science Drive, Newport, OR 97365, USA.
B Fisheries and Aquatic Sciences Program, School of Forest Resources and Conservation, University of Florida, 118 Newins-Ziegler Hall, PO Box 110410, Gainesville, FL 32611-0410, USA.
C Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039, USA.
D Marine Ecology and Conservation Laboratory, Federal University of São Paulo, Rua Dr Carvalho de Mendonça, 144, Encruzilhada, Santos, SP, CEP 11070-100, Brazil.
E Elasmobranch Laboratory, Biosciences Institute, Sao Paulo State University, Praça Infante Dom Henrique, s/n, Parque Bitarú, São Vicente, SP, CEP 11380-972, Brazil.
F Corresponding author. Email: fcaltabellotta@ufl.edu
Marine and Freshwater Research - https://doi.org/10.1071/MF19370
Submitted: 27 November 2019 Accepted: 6 July 2020 Published online: 20 August 2020
Abstract
Owing to poorly mineralising structures, ageing deep-water elasmobranchs requires unconventional techniques. The aim of the present study was to develop an ageing method for the goblin shark Mitsukurina owstoni (Jordan, 1898) using Alcian blue staining of the vertebral column. One vertebral centrum from a male individual measuring 315.2-cm total length (TL) was aged with a minimum age of 27 years. Using a Bayesian von Bertalanffy growth model informed by back-calculated length at age, a literature search of maximum male TL, the TL of the smallest free-swimming individuals and informative priors, we estimated males grow to 374 cm TL, mature at 16 years and live up to 60 years. Our results provide useful life history information, with the aim of elucidating the cryptic biology of this deep-water shark.
Keywords: Bayesian age–growth, deep-water elasmobranchs, goblin shark, Mitsukurina owstoni.
References
Baje, L., Smart, J. J., Chin, A., White, W. T., and Simpfendorfer, C. A. (2018). Age, growth and maturity of the Australian sharpnose shark Rhizoprionodon taylori from the Gulf of Papue. PLoS One 13, e0206581.| Age, growth and maturity of the Australian sharpnose shark Rhizoprionodon taylori from the Gulf of Papue.Crossref | GoogleScholarGoogle Scholar | 30379918PubMed |
Beverton, R. J. H., and Holt, S. J. (1959). A review of the lifespans and mortality rates of fish in nature, and their relation to growth and other physiological characteristics. In ‘Ciba Foundation Symposium – The Lifespan of Animals (Colloquia on Ageing)’. (Eds G. E. W. Wolstenholme and M. O’Connor.) pp. 142–180. (Wiley.)
Brooks, M., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. A., Nielsen, A., Skaug, H. J., Mächler, M., and Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378–400.
| glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling.Crossref | GoogleScholarGoogle Scholar |
Cadenat, J., and Blanche, J. (1981). ‘Requins de Méditerranée et d’Atlantique. Faune Tropicale.’ (Office de la Recherche Scientifique et Technique: Paris, France.)
Cailliet, G. M. (2015). Perspectives on elasmobranch life-history studies: a focus on age validation and relevance to fishery management. Journal of Fish Biology 87, 1271–1292.
| Perspectives on elasmobranch life-history studies: a focus on age validation and relevance to fishery management.Crossref | GoogleScholarGoogle Scholar | 26709208PubMed |
Cailliet, G. M., and Goldman, K. J. (2004). Age determination and validation in chondrichthyan fishes. In ‘Biology of Sharks and Their Relatives’. (Eds J. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 404–453. (CRC Press: 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 |
Caltabellotta, F. P., Silva, F. M., Motta, F. S., and Gadig, O. B. F. (2019a). Age and growth of the Rioraja agassizii (Chondrichthyes, Arhynchobatidae) in the western South Atlantic. Marine and Freshwater Research 70, 84–92.
| Age and growth of the Rioraja agassizii (Chondrichthyes, Arhynchobatidae) in the western South Atlantic.Crossref | GoogleScholarGoogle Scholar |
Caltabellotta, F. P., Siders, Z. A., Murie, D. J., Motta, F. S., Cailliet, G. M., and Gadig, O. B. F. (2019b). Age and growth of three endemic threatened guitarfishes Pseudobatos horkelii, P. percellens and Zapteryx brevirostris in the western South Atlantic Ocean. Journal of Fish Biology 95, 1236–1248.
| Age and growth of three endemic threatened guitarfishes Pseudobatos horkelii, P. percellens and Zapteryx brevirostris in the western South Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 31429078PubMed |
Caltabellotta, F. P., Siders, Z. A., Motta, F. S., Cailliet, G. M., and Gadig, O. B. F. (2020). First study on age and growth of the deep-water goblin shark, Mitsukurina owstoni (Jordan, 1898). bioRxiv , 2020.02.04.934281.
| First study on age and growth of the deep-water goblin shark, Mitsukurina owstoni (Jordan, 1898).Crossref | GoogleScholarGoogle Scholar |
Castro, J. I. (2011). ‘The Sharks of North America’, 1st edn. (Oxford University Press: New York, NY, USA.)
Charnov, E. L., Gislason, H., and Pope, J. G. (2013). Evolutionary assembly rules for fish life histories. Fish and Fisheries 14, 213–224.
| Evolutionary assembly rules for fish life histories.Crossref | GoogleScholarGoogle Scholar |
Compagno, L. J. V. (2001). ‘Sharks of the World: an Annotated and Illustrated Catalogue of Shark Species Known to Date. Volume 2: Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes)’, FAO Species Catalogue for Fishery Purposes number 1. (Food and Agriculture Organization of the United Nations: Rome, Italy.)
Cotton, C. F., and Grubbs, R. D. (2015). Biology of deep-water chondrichthyans: introduction. Deep-sea Research – II. Topical Studies in Oceanography 115, 1–10.
| Biology of deep-water chondrichthyans: introduction.Crossref | GoogleScholarGoogle Scholar |
Cotton, C. F., Grubbs, R. D., Daly-Engel, T. S., Lynch, P. D., and Musick, J. A. (2011). Age, growth and reproduction of a common deep-water shark, shortspine spurdog (Squalus cf. mitsukurii), from Hawaiian waters. Marine and Freshwater Research 62, 811–822.
| Age, growth and reproduction of a common deep-water shark, shortspine spurdog (Squalus cf. mitsukurii), from Hawaiian waters.Crossref | GoogleScholarGoogle Scholar |
Cotton, C. F., Andrews, A. H., Cailliet, G. M., Grubbs, R. D., Irvine, S. B., and Musick, J. A. (2014). Assessment of radiometric dating for age validation of deep-water dogfish (Order: Squaliformes) finspines. Fisheries Research 151, 107–113.
| Assessment of radiometric dating for age validation of deep-water dogfish (Order: Squaliformes) finspines.Crossref | GoogleScholarGoogle Scholar |
Dulvy, N. K., Simpfendorfer, C. A., Davidson, L. N., Fordham, S. V., Bräutigam, A., Sant, G., and Welch, D. J. (2017). Challenges and priorities in shark and ray conservation. Current Biology 27, R565–R572.
| Challenges and priorities in shark and ray conservation.Crossref | GoogleScholarGoogle Scholar | 28586694PubMed |
Farrell, E. D., Mariani, S., and Clarke, M. W. (2010). Age and growth estimates for the starry smoothhound (Mustelus asterias) in the northeast Atlantic Ocean. ICES Journal of Marine Science 67, 931–939.
| Age and growth estimates for the starry smoothhound (Mustelus asterias) in the northeast Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Finucci, B., and Duffy, C. A. J. (2018). Mitsukurina owstoni. In ‘IUCN Red List of Threatened Species 2018’, e.T44565A2994832. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/44565/2994832 [Verified 8 July 2020].
Francis, R. (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., Jones, E. G., Ó Maolagáin, C., and Lyon, W. S. (2018). Growth and reproduction of four deepwater sharks in New Zealand waters. New Zealand aquatic environment and biodiversity report number 196. (Ministry for Primary Industries: Wellington, New Zealand.) Available at https://www.fisheries.govt.nz/dmsdocument/27585/direct [Verified 20 July 2020].
Gallagher, M. J., Green, M. J., and Nolan, C. P. (2006). The potential use of caudal thorns as a non-invasive ageing structure in the thorny skate (Amblyraja radiata Donovan, 1808). Environmental Biology of Fishes 77, 265–272.
| The potential use of caudal thorns as a non-invasive ageing structure in the thorny skate (Amblyraja radiata Donovan, 1808).Crossref | GoogleScholarGoogle Scholar |
Gelman, A., and Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–472.
| Inference from iterative simulation using multiple sequences.Crossref | GoogleScholarGoogle Scholar |
Gelman, A., Simpson, D., and Betancourt, M. (2017). The prior can often only be understood in the context of the likelihood. Entropy 19, 555–568.
| The prior can often only be understood in the context of the likelihood.Crossref | GoogleScholarGoogle Scholar |
Geraghty, P. T., Macbeth, W. G., Harry, A. V., Bell, J. E., Yerman, M. N., and Williamson, J. E. (2014). Age and growth parameters for three heavily exploited shark species off temperate eastern Australia. ICES Journal of Marine Science 71, 559–573.
| Age and growth parameters for three heavily exploited shark species off temperate eastern Australia.Crossref | GoogleScholarGoogle Scholar |
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. Biodiversity, Adaptive Physiology, and Conservation’. (Eds J. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 423–452. (CRC Press: Boca Raton, FL, USA.)
Harry, A. V. (2018). Evidence for systemic age underestimation in shark and ray ageing studies. Fish and Fisheries 19, 185–200.
| Evidence for systemic age underestimation in shark and ray ageing studies.Crossref | GoogleScholarGoogle Scholar |
Henderson, A. C., Arkhipkin, A. I., and Chtcherbich, J. N. (2005). Distribution, growth and reproduction of the white-spotted skate Bathyraja albomaculata (Norman, 1937) around the Falkland Islands. Journal of Northwest Atlantic Fishery Science 35, 79–87.
| Distribution, growth and reproduction of the white-spotted skate Bathyraja albomaculata (Norman, 1937) around the Falkland Islands.Crossref | GoogleScholarGoogle Scholar |
Hewitt, D. A., and Hoenig, J. M. (2005). Comparison of two approaches for estimating natural mortality based on longevity. Fishery Bulletin 103, 433–437.
Holanda, F. C. A. F., and Asano-Filho, M. (2008). Registro da ocorrência do tubarão-duende, Mitsukurina owstoni Jordan, 1898 (Lamniformes: Mitsukurinidae) na região norte do Brasil. Arquivos de Ciências do Mar 41, 101–104.
Irvine, S. B., Stevens, J. D., and Laurenson, L. J. B. (2006). Comparing external and internal dorsal-spine bands to interpret the age and growth of the giant lantern shark, Etmopterus baxteri (Squaliformes: Etmopteridae). Developments in Environmental Biology of Fishes 25, 253–264.
| Comparing external and internal dorsal-spine bands to interpret the age and growth of the giant lantern shark, Etmopterus baxteri (Squaliformes: Etmopteridae).Crossref | GoogleScholarGoogle Scholar |
Jensen, A. L. (1996). Beverton and Holt life history invariants result from optimal trade-off of reproduction and survival. Canadian Journal of Fisheries and Aquatic Sciences 53, 820–822.
| Beverton and Holt life history invariants result from optimal trade-off of reproduction and survival.Crossref | GoogleScholarGoogle Scholar |
Kukuev, E. I. (1982). Fish fauna of the Corner Mountains and New England Submarine Ridge in the western North Atlantic. In ‘Maloizuchennye ryby otkrytogo okeana’. pp. 92–109. (P. P. Shirshov Institute of Oceanology: Moscow, USSR.) [In Russian].
Kurata, Y. (1967). Catch record of goblin shark (Scapanorynchus owstoni). Saishu-to-shiiku 29, 417.
Kyne, P. M., and Simpfendorfer, C. A. (2010). Deepwater chondrichthyans. In ‘Biology of Sharks and their Relatives II. Biodiversity, Adaptive Physiology, and Conservation’. (Eds J. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 37–113. (CRC Press: Boca Raton, FL, USA.)
Masai, H., Sato, Y., and Aoki, M. (1973). The brain of Mitsukurina owstoni. Journal für Hirnforschung 14, 493–500.
| 4792175PubMed |
Millar, R. B. (2002). Reference priors for Bayesian fisheries models. Canadian Journal of Fisheries and Aquatic Sciences 59, 1492–1502.
| Reference priors for Bayesian fisheries models.Crossref | GoogleScholarGoogle Scholar |
Natanson, L. J., Skomal, G. B., Hoffmann, S. L., Porter, M. E., Goldman, K. J., and Serra, D. (2018). Age and growth of sharks: do vertebral band pairs record age? Marine and Freshwater Research 69, 1440–1452.
| Age and growth of sharks: do vertebral band pairs record age?Crossref | GoogleScholarGoogle Scholar |
Noden, R. G. (1984). Another goblin. Australian Fisheries 43, 56.
Parsons, G. R., Ingram, G. W., and Havard, R. (2002). First record of the goblin shark Mitsukurina owstoni, Jordan (family Mitsukurinidae) in the Gulf of Mexico. Southeastern Naturalist 1, 189–192.
| First record of the goblin shark Mitsukurina owstoni, Jordan (family Mitsukurinidae) in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Piotrovskiy, A., and Prut’ko, V. (1980). The occurrence of the goblin shark, Scapanorhynchus owstoni (Chondrichthyes, Scapanorhynchidae), in the Indian Ocean. Journal of Ichthyology 20, 124–125.
Prince, J., Hordyk, A., Valencia, S. R., Loneragan, N., and Sainsbury, K. (2015). Revisiting the concept of Beverton–Holt life-history invariants with the aim of informing data-poor fisheries assessment. ICES Journal of Marine Science 72, 194–203.
| Revisiting the concept of Beverton–Holt life-history invariants with the aim of informing data-poor fisheries assessment.Crossref | GoogleScholarGoogle Scholar |
Ricker, W. E. (1979). Growth rates and models. In ‘Fish Physiology, III, Bioenergetics and Growth’. (Eds W. S. Hoar, D. J. Randall, and J. R. Brett.) pp. 677–743. (Academic Press: New York, NY, USA.)
Rigby, C., and Simpfendorfer, C. A. (2015). Patterns in life history traits of deep-water chondrichthyans. Deep-sea Research – II. Topical Studies in Oceanography 115, 30–40.
| Patterns in life history traits of deep-water chondrichthyans.Crossref | GoogleScholarGoogle Scholar |
Rigby, C. L., Wedding, B. B., Grauf, S., and Simpfendorfer, C. A. (2014). The utility of near infrared spectroscopy for age estimation of deepwater sharks. Deep-sea Research – I. Oceanographic Research Papers 94, 184–194.
| The utility of near infrared spectroscopy for age estimation of deepwater sharks.Crossref | GoogleScholarGoogle Scholar |
Rincon, G., Vaske, T., and Gadig, O. B. (2012). Record of the goblin shark Mitsukurina owstoni (Chondrichthyes: Lamniformes: Mitsukurinidae) from the South-Western Atlantic. Marine Biodiversity Records 5, e44.
| Record of the goblin shark Mitsukurina owstoni (Chondrichthyes: Lamniformes: Mitsukurinidae) from the South-Western Atlantic.Crossref | GoogleScholarGoogle Scholar |
Rincon, G., Mazzoleni, R. C., Palmeira, A. R. O., and Lessa, R. (2017). Deep-water sharks, rays, and chimaeras of Brazil. In ‘Chondrichthyes: Multidisciplinary Approach’. (Eds L. F. Rodrigues-Filho and J. B. D. L. Sales.) pp. 83–112. (IntechOpen: London, UK.)
Song, J., and Parenti, L. R. (1995). Clearing and staining whole fish specimens for simultaneous demonstration of bone, cartilage, and nerves. Copeia , 114–118.
| Clearing and staining whole fish specimens for simultaneous demonstration of bone, cartilage, and nerves.Crossref | GoogleScholarGoogle Scholar |
Stevens, J., and Paxton, J. (1985). A new record of the goblin shark, Mitsukurina owstoni (family Mitsukurinidae), from eastern Australia. Proceedings of the Linnean Society of New South Wales 108, 37–45.
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 | GoogleScholarGoogle Scholar |
Taylor, C. C. (1958). Cod growth and temperature. ICES Journal of Marine Science 23, 366–370.
| Cod growth and temperature.Crossref | GoogleScholarGoogle Scholar |
Ugoretz, J., and Siegel, J. (1999). First Eastern Pacific record of the goblin shark, Mitsukurina owstoni (Lamniformes: Mitsukurinidae). California Fish and Game 85, 118–120.
von Bertalanffy, L. (1934). Untersuchungen Über die Gesetzlichkeit des Wachstums: I. Teil: Allgemeine Grundlagen der Theorie; Mathematische und physiologische Gesetzlichkeiten des Wachstums bei Wassertieren. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen 131, 613–652.
| 28353935PubMed |
Yanagisawa, F. (1991). Notes on the oral morphology of goblin shark, Mitsukurina owstoni Jordan. Nanki Seibutsu 33, 10–14.
Yano, K., Miya, M., Aizawa, M., and Noichi, T. (2007). Some aspects of the biology of the goblin shark, Mitsukurina owstoni, collected from the Tokyo submarine canyon and adjacent waters, Japan. Ichthyological Research 54, 388–398.
| Some aspects of the biology of the goblin shark, Mitsukurina owstoni, collected from the Tokyo submarine canyon and adjacent waters, Japan.Crossref | GoogleScholarGoogle Scholar |
