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

Filling gaps in the biology and habitat use of two spurdog sharks (Squalus japonicus and Squalus brevirostris) in the East China Sea

Toshikazu Yano https://orcid.org/0000-0002-5866-7444 A C , Seiji Ohshimo B , Takeshi Sakai B and Mari Yoda B
+ Author Affiliations
- Author Affiliations

A National Fisheries University, Japan Fisheries Research and Education Agency, 2-7-1 Nagata-honmachi, Shimonoseki, Yamaguchi 759-6595, Japan.

B Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, 1551-8 Taira-machi, Nagasaki, Nagasaki 851-2213, Japan.

C Corresponding author. Email: tskzyn@fish-u.ac.jp

Marine and Freshwater Research 71(12) 1719-1731 https://doi.org/10.1071/MF19131
Submitted: 13 April 2019  Accepted: 24 February 2020   Published: 24 March 2020

Abstract

The conservation and management of sharks requires appropriate information on their biological and habitat characteristics. Data needed for the conservation and management of two dominant demersal shark species in the East China Sea, the spurdogs (Squalus japonicus and Squalus brevirostris), are inadequate. To remedy this, we analysed biological, catch and abiotic data from bottom trawl surveys conducted in 2000–05 and 2008–14 from within the East China Sea. The precaudal length of male and female S. japonicus at 50% sexual maturity was 396.1 and 459.9 mm respectively, whereas for S. brevirostris it was 289.6 and 354.9 mm respectively. Prey overlap was high between species, with lanternfishes the most important prey. The fractional trophic level was 4.33 for S. japonicus and 4.31 for S. brevirostris. We estimated spurdog habitat using a generalised additive model. Depth affected the presence of both sharks, with latitude also affecting the presence of S. brevirostris. These two spurdog species were spatially segregated over the continental slope, and body-length and sex-ratio distributions suggested that there was a maturity-based segregation within and among species. The results of this study improve our understanding of the population dynamics of these spurdog species, their reproduction and diet, fundamental information required for their conservation and for improved fisheries management.

Additional keywords: habitat model, Japanese shortnose spurdog, Japanese spurdog, mating season, stable isotopes.


References

Baum, J. K., and Worm, B. (2009). Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78, 699–714.
Cascading top-down effects of changing oceanic predator abundances.Crossref | GoogleScholarGoogle Scholar | 19298616PubMed |

Camhi, M., Fowler, S., Musick, J., Bräutigam, A., and Fordham, S. (1998). ‘Sharks and their Relatives – Ecology and Conservation.’ (IUCN: Gland, Switzerland, and Cambridge, UK.)

Carlisle, A. B., Litvin, S. Y., Madigan, D. J., Lyons, K., Bigman, J. S., Ibarra, M., and Bizzarro, J. J. (2017). Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 74, 419–428.
Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |

Chen, C., Taniuchi, T., and Nose, Y. (1981). Some aspects of reproduction in the pointed-snout dogfish Squalus japonicus taken off Nagasaki and Choshi. Nippon Suisan Gakkaishi 47, 1157–1164.
Some aspects of reproduction in the pointed-snout dogfish Squalus japonicus taken off Nagasaki and Choshi.Crossref | GoogleScholarGoogle Scholar |

Cheng, J., Cheung, W. W. L., and Pitcher, T. J. (2009). Mass-balance ecosystem model of the East China Sea. Progress in Natural Science 19, 1271–1280.
Mass-balance ecosystem model of the East China Sea.Crossref | GoogleScholarGoogle Scholar |

Coll, M., Libralato, S., Tudela, S., Palomera, I., and Pranovi, F. (2008). Ecosystem overfishing in the ocean. PLoS One 3, e3881.
Ecosystem overfishing in the ocean.Crossref | GoogleScholarGoogle Scholar | 19066624PubMed |

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. (Food and Agriculture Organization of the United Nations: Rome, Italy.) Available at http://www.fao.org/3/ad122e/ad122e00.htm [Verified 25 February 2020].

Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.
A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |

Dell’Apa, A., Cudney-Burch, J., Kimmel, D. G., and Rulifson, R. A. (2014). Sexual segregation of spiny dogfish in fishery-dependent surveys in Cape Cod, Massachusetts: potential management benefits. Transactions of the American Fisheries Society 143, 833–844.
Sexual segregation of spiny dogfish in fishery-dependent surveys in Cape Cod, Massachusetts: potential management benefits.Crossref | GoogleScholarGoogle Scholar |

Dell’Apa, A., Bangley, C. W., and Rulifson, R. A. (2015). Who let the dogfish out? A review of management and socio-economic aspects of spiny dogfish fisheries. Reviews in Fish Biology and Fisheries 25, 273–295.
Who let the dogfish out? A review of management and socio-economic aspects of spiny dogfish fisheries.Crossref | GoogleScholarGoogle Scholar |

DeNiro, M. J., and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.Crossref | GoogleScholarGoogle Scholar |

DeNiro, M. J., and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
Influence of diet on the distribution of nitrogen isotopes in animals.Crossref | GoogleScholarGoogle Scholar |

Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J. V., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S., and White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |

Ferry, L. A., Clark, S. L., and Cailliet, G. M. (1997). Food habits of spotted sand bass (Paralabrax maculatofasciatus, Serranidae) from Bahia de Los Angeles, Baja California. Bulletin of the Southern California Academy of Sciences 96, 1–21.

Hanley, J. A., and McNeil, B. J. (1982). The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143, 29–36.
The meaning and use of the area under a receiver operating characteristic (ROC) curve.Crossref | GoogleScholarGoogle Scholar | 7063747PubMed |

Haugen, J. B., Curtis, T. H., Fernandes, P. G., Sosebee, K. A., and Rago, P. J. (2017). Sexual segregation of spiny dogfish (Squalus acanthias) off the northeastern United States: implications for a male-directed fishery. Fisheries Research 193, 121–128.
Sexual segregation of spiny dogfish (Squalus acanthias) off the northeastern United States: implications for a male-directed fishery.Crossref | GoogleScholarGoogle Scholar |

Hoenig, J. M., and Gruber, S. H. (1990). Life-history patterns in the elasmobranchs: implications for fisheries management. In ‘Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries’. (Eds H. L. Pratt Jr, S. H. Gruber, and T. Taniuchi.) NOAA Technical Report NMFS 90, pp. 1–16. (US Department of Commerce, National Oceanic and Atmospheric Administration: Silver Spring, MD, USA.)

Holden, M. J. (1974). Problems in the rational exploitation of elasmobranch populations and some suggested solutions. In ‘Sea Fisheries Research’. (Ed. F. R. Harden-Jones.) pp. 117–137. (Paul Elek: London, UK.)

Kai, M., Shiozaki, K., Ohshimo, S., and Yokawa, K. (2015). Growth and spatiotemporal distribution of juvenile shortfin mako (Isurus oxyrinchus) in the western and central North Pacific. Marine and Freshwater Research 66, 1176–1190.
Growth and spatiotemporal distribution of juvenile shortfin mako (Isurus oxyrinchus) in the western and central North Pacific.Crossref | GoogleScholarGoogle Scholar |

Kibesaki, O. (1954). Studies on the sharks from the East China and Yellow Seas (II): maturity of the S. brevirostris. In ‘Bulletin of the Seikai Regional Fisheries Research Laboratory 5’. pp 36–46. (Seikai Regional Fisheries Research Laboratory: Nagasaki, Japan.) [In Japanese with an English abstract].

Kim, S. L., and Koch, P. L. (2012). Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes 95, 53–63.
Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Kousteni, V., Karachle, P. K., and Megalofonou, P. (2017). Diet and trophic level of the longnose spurdog Squalus blainville (Risso, 1826) in the deep waters of the Aegean Sea. Deep-sea Research – I. Oceanographic Research Papers 124, 93–102.
Diet and trophic level of the longnose spurdog Squalus blainville (Risso, 1826) in the deep waters of the Aegean Sea.Crossref | GoogleScholarGoogle Scholar |

Kudo, S. (1956). A study of Japanese shortnose spurdog (Squalus brevirostris Tanaka) in Hyuga-nada, Japan. In ‘Report of Nankai Regional Fisheries Research Laboratory 3’. pp. 66–72. (Nankai Regional Fisheries Research Laboratory: Kochi, Japan.) [In Japanese].

Linton, L. R., Davies, R. W., and Wrona, F. J. (1981). Resource utilization indices: an assessment. Journal of Animal Ecology 50, 283–292.
Resource utilization indices: an assessment.Crossref | GoogleScholarGoogle Scholar |

MacNeil, M. A., Skomal, G. B., and Fisk, A. T. (2005). Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series 302, 199–206.
Stable isotopes from multiple tissues reveal diet switching in sharks.Crossref | GoogleScholarGoogle Scholar |

Mandelman, J. W., and Farrington, M. A. (2007). The physiological status and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch, Squalus acanthias. ICES Journal of Marine Science 64, 122–130.
The physiological status and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch, Squalus acanthias.Crossref | GoogleScholarGoogle Scholar |

Metz, C. E. (1978). Basic principles of ROC analysis. Seminars in Nuclear Medicine 8, 283–298.
Basic principles of ROC analysis.Crossref | GoogleScholarGoogle Scholar | 112681PubMed |

Molinero, A., and Flos, R. (1992). Influence of season on the feeding habits of the common sole Solea solea. Marine Biology 113, 499–507.
Influence of season on the feeding habits of the common sole Solea solea.Crossref | GoogleScholarGoogle Scholar |

Morgan, J. A. T., Harry, A. V., Welch, D. J., Street, R., White, J., Geraghty, P. T., Macbeth, W. G., Tobin, A., Simpfendorfer, C. A., and Ovenden, J. R. (2012). Detection of interspecies hybridisation in Chondrichthyes: hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery. Conservation Genetics 13, 455–463.
Detection of interspecies hybridisation in Chondrichthyes: hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery.Crossref | GoogleScholarGoogle Scholar |

Moura, T., Jones, E., Clarke, M. W., Cotton, C. F., Crozier, P., Daley, R. K., Diez, G., Dobby, H., Dyb, J. E., Fossen, I., Irvine, S. B., Jakobsdottir, K., López-Abellán, L. J., Lorance, P., Pascual-Alayón, P., Severino, R. B., and Figueiredo, I. (2014). Large-scale distribution of three deep-water squaloid sharks: integrating data on sex, maturity and environment. Fisheries Research 157, 47–61.
Large-scale distribution of three deep-water squaloid sharks: integrating data on sex, maturity and environment.Crossref | GoogleScholarGoogle Scholar |

Mucientes, G. R., Queiroz, N., Sousa, L. L., Tarroso, P., and Sims, D. W. (2009). Sexual segregation of pelagic sharks and the potential threat from fisheries. Biology Letters 5, 156–159.
Sexual segregation of pelagic sharks and the potential threat from fisheries.Crossref | GoogleScholarGoogle Scholar | 19324655PubMed |

Nakano, H. (1994). Age, reproduction and migration of blue shark in the North Pacific Ocean. In ‘Bulletin of National Research Institute of Far Seas Fisheries 31’. pp. 141–256. (National Research Institute of Far Seas Fisheries: Shizuoka, Japan.) [In Japanese with an English abstract].

Ohshimo, S., Yasuda, T., Tanaka, H., and Sassa, C. (2012). Biomass fluctuation of two dominant lanternfish Diaphus garmani and D. chrysorhynchus with environmental changes in the East China Sea. Fisheries Science 78, 33–39.
Biomass fluctuation of two dominant lanternfish Diaphus garmani and D. chrysorhynchus with environmental changes in the East China Sea.Crossref | GoogleScholarGoogle Scholar |

Ohshimo, S., Tanaka, H., Nishiuchi, K., and Yasuda, T. (2016). Trophic positions and predator–prey mass ratio of the pelagic food web in the East China Sea and Sea of Japan. Marine and Freshwater Research 67, 1692–1699.
Trophic positions and predator–prey mass ratio of the pelagic food web in the East China Sea and Sea of Japan.Crossref | GoogleScholarGoogle Scholar |

Pauly, D., and Palomares, M. L. (2005). Fishing down marine food web: it is far more pervasive than we thought. Bulletin of Marine Science 76, 197–211.

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Pratt, H. L., and Carrier, J. C. (2001). A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes 60, 157–188.
A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum.Crossref | GoogleScholarGoogle Scholar |

Sagarese, S. R., Frisk, M. G., Cerrato, R. M., Sosebee, K. A., Musick, J. A., and Rago, P. J. (2014). Application of generalized additive models to examine ontogenetic and seasonal distributions of spiny dogfish (Squalus acanthias) in the northeast (US) shelf large marine ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 71, 847–877.
Application of generalized additive models to examine ontogenetic and seasonal distributions of spiny dogfish (Squalus acanthias) in the northeast (US) shelf large marine ecosystem.Crossref | GoogleScholarGoogle Scholar |

Sato, S. (1935). A note on the Pacific dog fish (Squalus suckleyi Girard) in the coastal waters of Hokkaido, Japan. Journal of the Faculty of Science, Hokkaido Imperial University – 6. Zoology 4, 127–141.

Schoeninger, M. J., and DeNiro, M. J. (1984). Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48, 625–639.
Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals.Crossref | GoogleScholarGoogle Scholar |

Simpfendorfer, C. A., Heupel, M. R., White, W. T., and Dulvy, N. K. (2011). The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Marine and Freshwater Research 62, 518–527.
The importance of research and public opinion to conservation management of sharks and rays: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Smith, S. E., Au, D. W., and Show, C. (1998). Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678.
Intrinsic rebound potentials of 26 species of Pacific sharks.Crossref | GoogleScholarGoogle Scholar |

Sosebee, K. A. (2005). Are density-dependent effects on Elasmobranch maturity possible? Journal of Northwest Atlantic Fishery Science 35, 115–124.
Are density-dependent effects on Elasmobranch maturity possible?Crossref | GoogleScholarGoogle Scholar |

Sulikowski, J. A., Galuardi, B., Bubley, W., Furey, N. B., Driggers, W. B., Ingram, G. W., and Tsang, P. C. W. (2010). Use of satellite tags to reveal the movements of spiny dogfish Squalus acanthias in the western North Atlantic Ocean. Marine Ecology Progress Series 418, 249–254.
Use of satellite tags to reveal the movements of spiny dogfish Squalus acanthias in the western North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Swets, J. A. (1988). Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.
Measuring the accuracy of diagnostic systems.Crossref | GoogleScholarGoogle Scholar | 3287615PubMed |

Tanaka, S., and McCormack, C. (2009). Japanese spurdog Squalus japonicus. In ‘The IUCN Red List of Threatened Species 2009’. e.T161433A5422974. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK.) Available at https://www.iucnredlist.org/species/161433/5422974 [Verified 25 February 2020].

Taylor, I. G., and Gallucci, V. F. (2009). Unconfounding the effects of climate and density dependence using 60 years of data on spiny dogfish (Squalus acanthias). Canadian Journal of Fisheries and Aquatic Sciences 66, 351–366.
Unconfounding the effects of climate and density dependence using 60 years of data on spiny dogfish (Squalus acanthias).Crossref | GoogleScholarGoogle Scholar |

Tribuzio, C. A., Strasburger, W. W., and Kruse, G. H. (2017). Do abiotic and ontogenetic factors influence the diet of a generalist predator? Feeding ecology of the Pacific spiny dogfish (Squalus suckleyi) in the northeast Pacific Ocean. Environmental Biology of Fishes 100, 685–701.
Do abiotic and ontogenetic factors influence the diet of a generalist predator? Feeding ecology of the Pacific spiny dogfish (Squalus suckleyi) in the northeast Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Wallace, R. K., and Ramsey, J. S. (1983). Reliability in measuring diet overlap. Canadian Journal of Fisheries and Aquatic Sciences 40, 347–351.
Reliability in measuring diet overlap.Crossref | GoogleScholarGoogle Scholar |

White, W. T. (2009). Japanese shortnose spurdog Squalus brevirostris. In ‘The IUCN Red List of Threatened Species 2009’. e.T161438A5423985. (International Union for Conservation of Nature and Natural Resources: Cambridge, UK.) Available at https://www.iucnredlist.org/species/161438/5423985 [Verified 25 February 2020].

Yamada, U., Tokimura, M., Horikawa, H., and Nakabo, T. (2007). ‘Fishes and Fisheries of the East China and Yellow Seas.’ (Tokai University Press: Kanagawa, Japan.) [In Japanese].

Yamamoto, K., and Nagasawa, K. (2013). Benthic shrimp assemblages associated with water masses in the East China Sea and the Yellow Sea. Nippon Suisan Gakkaishi 79, 987–1001.
Benthic shrimp assemblages associated with water masses in the East China Sea and the Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Yamamoto, K., and Nagasawa, K. (2015). Species composition of crabs and change in abundance of portunid crabs in the East China Sea and the Yellow Sea from the 1990s to 2000s. Nippon Suisan Gakkaishi 81, 43–51.
Species composition of crabs and change in abundance of portunid crabs in the East China Sea and the Yellow Sea from the 1990s to 2000s.Crossref | GoogleScholarGoogle Scholar |

Yano, K., and Kugai, K. (1993). Deep-sea chondrichthyans collected from the waters around the Okinawa Islands: results of catch analysis of bottom longlines. In ‘Bulletin of Seikai National Fisheries Research Institute 71’. pp. 51–65. (Seikai National Fisheries Research Institute: Nagasaki, Japan.) [In Japanese with an English abstract].

Yano, K., and Tanaka, S. (1984). Review of the deep sea squaloid shark genus Scymnodon of Japan, with a description of a new species. Japanese Journal of Ichthyology 30, 341–360.
Review of the deep sea squaloid shark genus Scymnodon of Japan, with a description of a new species.Crossref | GoogleScholarGoogle Scholar |

Yano, K., and Tanaka, S. (1988). Size at maturity, reproductive cycle, fecundity, and depth segregation of the deep sea squaloid sharks Centroscymnus owstoni and C. coelolepis in Suruga Bay, Japan. Nippon Suisan Gakkaishi 54, 167–174.
Size at maturity, reproductive cycle, fecundity, and depth segregation of the deep sea squaloid sharks Centroscymnus owstoni and C. coelolepis in Suruga Bay, Japan.Crossref | GoogleScholarGoogle Scholar |

Yano, T., Hattori, T., Tamukai, T., and Ohshimo, S. (2017a). Body-length frequency and spatial segregation of the North Pacific spiny dogfish Squalus suckleyi in Tsugaru Strait, northern Japan. Fisheries Science 83, 917–928.
Body-length frequency and spatial segregation of the North Pacific spiny dogfish Squalus suckleyi in Tsugaru Strait, northern Japan.Crossref | GoogleScholarGoogle Scholar |

Yano, T., Ohshimo, S., Kanaiwa, M., Hattori, T., Fukuwaka, M., Nagasawa, T., and Tanaka, S. (2017b). Spatial distribution analysis of the North Pacific spiny dogfish, Squalus suckleyi, in the North Pacific using generalized additive models. Fisheries Oceanography 26, 668–679.
Spatial distribution analysis of the North Pacific spiny dogfish, Squalus suckleyi, in the North Pacific using generalized additive models.Crossref | GoogleScholarGoogle Scholar |

Zhou, S., Yin, S., Thorson, J. T., Smith, A. D. M., and Fuller, M. (2012). Linking fishing mortality reference points to life history traits: an empirical study. Canadian Journal of Fisheries and Aquatic Sciences 69, 1292–1301.
Linking fishing mortality reference points to life history traits: an empirical study.Crossref | GoogleScholarGoogle Scholar |