Scientia Marina, Vol 78, No 2 (2014)

Stock identification of neon flying squid (Ommastrephes bartramii) in the North Pacific Ocean on the basis of beak and statolith morphology

Zhou Fang
College of Marine Sciences, Shanghai Ocean University, China

Bilin Liu
College of Marine Sciences, Shanghai Ocean University - The Key Laboratory of Shanghai Education Commission for Oceanic Fisheries Resources Exploitation - The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, China

Jianghua Li
College of Marine Sciences, Shanghai Ocean University - The Key Laboratory of Shanghai Education Commission for Oceanic Fisheries Resources Exploitation - The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, China

Hang Su
College of Marine Sciences, Shanghai Ocean University, China

Xinjun Chen
College of Marine Sciences, Shanghai Ocean University - The Key Laboratory of Shanghai Education Commission for Oceanic Fisheries Resources Exploitation - The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, China


Cephalopods are becoming increasingly important in global fisheries as a result of increased landings and are playing an important ecological role in the trophic dynamics of marine ecosystems. Ommastrephes bartramii is a pelagic cephalopod species with two widely distributed spawning stocks in the North Pacific Ocean. It is also a major fishing target for the Chinese squid jigging fleets. Successful separation of these two spawning stocks is critical to fisheries management, but tends to be challenging because of their similar morphology. In this study we attempted to identify the stocks based on discriminant analyses of 9 morphological variables of statolith and 12 variables of beaks measured for O. bartramii samples in the North Pacific. A significant difference was revealed in the standardized beak and statolith variables between sexes in the northeast (NE) stock (P < 0.05). The northwest (NW) stock showed significant differences between sexes for all variables (P < 0.05) except for upper wing length (P > 0.05), whereas the NW stock showed no significant difference in either sex for the statolith variables (P > 0.05). The same sex also revealed different patterns with different hard structures between the two stocks. In t-tests females showed significant differences between stocks in statolith morphology (P < 0.05) and beak morphology (P < 0.05); males also showed this difference between cohorts in statolith variables (P < 0.05) except dorsal dome length and wing length (P > 0.05), but showed no difference between cohorts (P > 0.05) in beak morphometric variables. With the combination of two standardized hard parts, correct classification of stepwise discriminant analysis (SDA) was raised by nearly 20% compared with using only one structure, although overlaps of the NW stock were still found in the scatter-plots. It is concluded that adding more appropriate hard structure variables will effectively increase the success of separating geographic stocks by the SDA method.


Ommastrephes bartramii; statolith; beaks; morphology; geographic stock; stepwise discriminant analysis

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Adkison M.D. 1995. Population differentiation in Pacific salmons: local adaptation genetic drift, or the environment? Can. J. Fish. Aquat. Sci. 52(12): 2762-2777.

Arkhipkin A.I. 2003. Towards identification of the ecological lifestyle in nektonic squid using statolith morphometry. J. Mollus. Stud. 69: 171-178.

Arkhipkin A.I. 2005. Statolith as black boxes (life recorders) in squid. Mar. Freshwater Res. 56(5): 573-583.

Arkhipkin A.I., Bizikov V.A. 2000. Role of the statolith in functioning of the acceleration receptor system in squids and sepioids. J. Zool. 250(1): 31-55.

Arkhipkin A.I., Shcherbich Z.N. 2012. Thirty years' progress in age determination of squid using statoliths. J. Mar. Biol. Ass. U. K. 92(06): 1389-1398.

Bizikov V. A., Arkhipkin A. I. 1997. Morphology and microstructure of the gladius and statolith from the boreal Pacific giant squid Moroteuthis robusta (Oegopsida; Onychoteuthidae). J. Zool. 241(3): 475-492.

Bower J.R., Ichii T. 2005. The red flying squid (Ommastrephes bartramii): A review of recent research and the fishery in Japan. Fish. Res. 76(1): 39-55.

Bower S.M., Margolis L. 1991. Potential use of helminth parasites in stock identification of flying squid, Ommastrephes bartramii, in North Pacific waters. Can. J. Zool. 69(4): 1124-1126.

Burke W.T., Freeberg M., Miles E.L. 1993. United Nations Resolutions on driftnet fishing: An unsustainable precedent for high seas and coastal fisheries management. Ocean Dev. Int. Law. 25: 127-186.

Cabanellas-Reboredo M., Alós J., Palmer M., et al. 2011. Simulating the indirect handline jigging effects on the European squid (Loligo vulgaris) in captivity. Fish. Res. 110(3): 435-440.

Cadrin S.X., Silva V.M. 2005. Morphometric variation of yellowtail flounder. ICES J. Mar. Sci. 62: 683-694.

Castanhari G., Tomás A.R.G. 2012. Beak increment counts as a tool for growth studies of the common octopus Octopus vulgaris in southern Brazil. Bol. Inst. Pesca, São Paulo 38(4): 323-331.

Chen C.S. 2010. Abundance trends of two neon flying squid (Ommastrephes bartramii) stocks in the North Pacific. ICES J. Mar. Sci. 67(7): 1336-1345.

Chen C.S., Chiu T.S. 2003. Variations of life history parameters in two geographical groups of the neon flying squid, Ommastrephes bartramii, from the North Pacific. Fish. Res. 63: 349-366.

Chen X.J., Tian S.Q., Ye X.C. 2002. Study on population structure of flying squid in Northwestern Pacific based on gray system theory. J. Shanghai Fish. Univ. 11(4): 335-341. (In Chinese with English Abstract)

Chen X.J., Liu B.L., Wang Y.G. 2009. Cephalopod of the world. Marine Press, Beijing, China, 1064 pp.

Chen X.J., Ma J., Liu B.L., et al. 2010. Effects of sexual maturity and body size on statolith shape of Ommastrephes bartramii in the Northwest Pacific Ocean. J. Fish. China. 30(6): 928-934. (In Chinese with English abstract)

Chen F., Chen X.J., Lu H.J., et al. 2011. Comparison of biological characteristics of Ommastrephes bartarmii between two different areas in the east central waters of North Pacific Ocean. J. Shanghai Fish. Univ. 20(5): 759-764. (In Chinese with English Abstract)

Chen X.J., Lu H.J., Liu B.L., et al. 2012. Species identification of Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis and Illex argentinus (Ommastrephidae) using beak morphological variables. Sci. Mar. 76(3): 473-481.

Chen X.J., Li J.H., Liu B.L., et al. 2013. Age, growth and population structure of Jumbo flying squid, Dosidicus gigas, off the Costa Rica Dome. J. Mar. Biol. Ass. U. K. 93:567-573

Cherel Y., Hobson K.A. 2005. Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc. R. Soc. Lond. B. 272: 1601-1607. PMid:16048776 PMCid:PMC1559839

Cherel Y., Ridoux V., Spitz J., et al. 2009. Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biol. Lett. 5: 364-367. PMid:19324634 PMCid:PMC2679927

Clarke M.R. 1962. The identification of cephalopod "beaks" and the relationship between beak size and total body weight. Bull. Br. Mus. nat. Hist. Zool. 8: 419-480

Clarke M.R. 1978. The cephalopod statolith-introduction to its form. J. Mar. Biol. Ass. U.K. 58: 701-712.

Clarke M.R. 1986. A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford, UK, 273 pp.

Clarke M.R. 2003. Potential of statoliths for interpreting coleoid evolution: a brief review. Ber. Palä. Abh. 3: 37-47.

Crespi-Abril A.C., Morsan E.M., Barón P.J. 2010. Analysis of the ontogenetic variation in body and beak shape of the Illex argentinus inner shelf spawning groups by geometric morphometrics. J. Mar. Biol. Ass. U. K. 90(03): 547-553.

Dommergues J.L., Neige P., Boletzky S.V. 2000. Exploration of morphospace using procrustes analysis in statoliths of cuttlefish and squid (Cephalopoda: Decabrachia)-evolutionary aspects of form disparity. Veliger-berkeley, 43(3): 265-276.

Durholtz M.D., Lipinski M.R., Przybylowicz W.J., et al. 1997. Nuclear microprobe mapping of statoliths of chokka squid Loligo vulgaris reynaudii d'Orbigny, 1845. Biol. Bull. 193(2): 125-140.

Fang Z., Chen X.J., Lu H.J., et al. 2012. Morphological differences in statolith and beak between two spawning stocks for Illex argentinus. Acta. Ecol. Sin. 32(19): 5986-5997. (In Chinese with English Abstract)

Francis R.I.C.C., Mattlin R.H. 1986. A possible pitfall in the morphometric application of discriminant analysis: measurement bias. Mar. Biol. 93(2): 311-313.

Guerra A., Rodríguez-navarro A.B., González A.F., et al. 2010. Life-history traits of the giant squid Architeuthis dux revealed from stable isotope signatures recorded in beaks. ICES J. Mar. Sci. 67(7): 1425-1431.

Hanlon R.T., Messenger J.B. 1996. Cephalopod Behaviour. Cambridge University Press Cambridge, UK, 232 pp. PMCid:PMC2271250

Ichii T., Mahapatra K., Sakai M., et al. 2004. Differing body size between the autumn and the winter-spring cohorts of neon flying squid (Ommastrephes bartramii) related to the oceanographic regime in the North Pacific: a hypothesis. Fish. Oceanogr. 13: 295-309

Ichii T., Mahapatra K., Sakai M., et al. 2009. Life history of the neon flying squid: effect of the oceanographic regime in the North Pacific Ocean. Mar. Ecol. Prog. Ser. 378: 1-11.

Ikeda Y., Arai N., Sakamoto W., et al. 1996. PIXE analysis of trace elements in squid statoliths: comparison between Ommastrephidae and Loliginidae. International Journal of PIXE. 6: 537-542.

Ikeda Y., Arai N., Sakamoto W., et al. 1997. Comparison on trace elements in squid statoliths of different species' origin as available key for taxonomic and phylogenetic study. International Journal of PIXE. 7: 141-146.

Ikeda Y., Arai N., Kidokoro H., et al. 2003. Strontium: calcium ratios in statoliths of Japanese common squid Todarodes pacificus (Cephalopoda: Ommastrephidae) as indicators of migratory behavior. Mar. Ecol. Prog. Ser. 251(1): 169-179.

Jackson G.D., Domeier M.L. 2003. The effects of an extraordinary El Ni-o/La Ni-a event on the size and growth of the squid Loligo opalescens off Southern California. Mar. Biol. 142(5): 925-935.

Katugin O.N. 2002. Patterns of genetic variability and population structure in the North Pacific squids Ommastrephes bartramii, Todarodes pacificus and Berryteuthis magister. Bull. Mar. Sci. 71(1): 383-420.

Kurosaka K., Yamashita H., Ogawa M., et al. 2012. Tentacle-breakage mechanism for the neon flying squid (Ommastrephes bartramii) during the jigging capture process. Fish. Res. 121: 9-16.

Lefkaditou E., Bekas P. 2004. Analysis of beak morphometry for the horned octopus Eledone cirrhosa (Cephalopoda: Octopoda) from the Thracian Sea (NE Mediterranean). Mediterr. Mar. Sci. 5(1): 143-149.

Lefkaditou E., Peristeraki P., Chartosia N., et al. 2011. Recent findings of Ommastrephes bartramii (Cephalopoda: Ommastrephidae) in the eastern Mediterranean and the implication on its range expansion. Mediterr. Mar. Sci. 12(2): 413-428.

Lipinski M. R., Underhill L. G. 1995. Sexual maturation in squid: quantum or continuum. S. Afr. J. Mar. Sci. 15: 207-223

Lleonart J., Salat J., Torres G.J. 2000. Removing allometric effects of body size in morphological analysis. J. Thero. Biol. 205: 85-93. PMid:10860702

Lombarte A., Sanchez P., Morales-Nin B. 1997. Intraspecific shape variability in statoliths of three cephalopod species. Vie Milieu 47: 165-169.

Lombarte A., Rufino M.M., Sánchez P. 2006. Statolith identification of Mediterranean Octopodidae, Sepiidae, Loliginidae, Ommastrephidae and Enoploteuthidae based on warp analyses. J. Mar. Biol. Ass. U. K. 86(04): 767-771.

Lu C.C., Ickeringill R. 2002. Cephalopod beak identification and biomass estimation techniques: tools for dietary studies of southern Australian finfishes. Mus. Victoria Sci. Rep. 6: 1-65.

Ma J., Chen X.J., Liu B.L., et al. 2009. Morphologic Features of Statolith for Ommastrephes bartramii in the Northwest Pacific Ocean. Periodical of Ocean University of China 39(2): 215-220. (In Chinese with English abstract)

Martínez P., Sanjuan A., Guerra A. 2002. Identification of Illex coindetii, I. illecebrosus and I. argentines (Cephalopoda: Ommastrephidae) throughout the Atlantic Ocean by body and beak characters. Mar. Biol. 141:131-143

Mercer M.C., Misra R.K., Hurley G.V. 1980. Sex determination of the Ommastrephid squid Illex illecebrosus using beak morphometric. Can. J. Fish. Aquat. Sci. 37: 283-286

Miserez A., Rubin D., Waite J.H. 2010. Cross-linking Chemistry of Squid Beak. J. Biol. Chem. 285(49): 38115-38124. PMid:20870720 PMCid:PMC2992245

Moltschaniwskyj N.A. 1995. Changes in shape associated with growth in the loliginid squid Photololigo sp.: a morphometric approach. Can. J. Zool. 73(7): 1335-1343.

Murakami K., Watanabe Y., Nakata J. 1981. Growth, distribution and migration of flying squid (Ommastrephes bartrami) in the North Pacific. In: Mishima, S. (ed.), Pelagic animals and environments around the Subarctic Boundary in North Pacific. Hokkaido University, Research Institute of North Pacific Fisheries, Hakodate, pp. 161-179 (In Japanese with English abstract)

Murata M. 1990. Oceanic resources of squids. Mar. Behav. Phys. 18: 19-71.

Murata M., Hayase S. 1993. Life history and biological information on flying squid (Ommastrephes bartramii) in the North Pacific Ocean. Bull. Int. Nat. North Pacific Comm. 53: l47-182.

Nagasawa K., Mori J., Okamura H. 1998. Parasites as biological tags of stocks of neon flying squid (Ommastrephes bartramii) in the North Pacific Ocean, In: Okutani, T. (1998), Contributed papers to International Symposium on Large Pelagic Squids, July 18-19, 1996, for JAMARC's 25th anniversary of its foundation, pp. 49-64.

Neige P. 2006. Morphometrics of hard structures in cuttlefish. Vie Milieu 56(2): 121-127.

Neige P., Dommergues, J.L. 2002. Disparity of beaks and statoliths of some coleoids a morphometric approach to depict shape differentiation. Gabh. der Geol. Bun. 57: 393-399

O'Dor R.K., Dawe E.G. 1998. Illex illecebrosus. In: Rodhouse P.G., Dawe E.G., O'Dor R.K. (eds), Squid recruitment dynamics. FAO Fish Tech Pap 376, Rome, pp. 77-104.

O'Dor R.K., Hoar J.A. 2000. Does geometry limit squid growth? ICES J. Mar. Sci. 57(1): 8-14.

Ogden R.S., Allcock A.L., Wats P.C., et al. 1998. The role of beak shape in octopodid taxonomy. S. Afr. J. Mar. Sci. 20(1): 29-36.

Perales-Raya C., Jurado-Ruzafa A., Bartolomé A., et al. 2014. Age of spent Octopus vulgaris and stress mark analysis using beaks of wild individuals. Hydrobiologia 725(1): 105-114.

Piatkowski U., K., Heinemann H. 2001. Cephalopod prey of king penguins (Aptenodytes patagonicus) breeding at Volunteer Beach, Falkland Islands, during austral winter 1996. Fish. Res. 52(1): 79-90.

Pierce G. J., Hastie L. C., Guerra A., et al. 1994. Morphometric variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fish. Res. 21(1): 127-148.

Pineda S.E., Hernández D.R., Brunetti N.E., et al. 2002. Morphological identification of two Southwest Atlantic Loliginid squids: Loligo gahi and Loligo sanpaulensis. Rev. Invest. Desarr. Pesq. 15: 67-84.

Raya C.P., Hernández-González C.L. 1998. Growth lines within the beak microstructure of the octopus Octopus vulgaris Cuvier, 1797. S. Afr. J. Mar. Sci. 20(1): 135-142.

Raya C.P., Bartolomé A., García-Santamaría M.T., et al. 2010. Age estimation obtained from analysis of octopus (Octopus vulgaris Cuvier, 1797) beaks: Improvement and comparisons. Fish. Res. 106: 171-176

Rencher A.C. 2002. Methods of Multivariate Analysis, 2nd edition. John Wiley & Sons, Inc, New York.

Rocha F., Guerra A., González A.F. 2001. A review of reproductive strategies in cephalopods. Biol. Rev. 76: 291-304. PMid:11569786

Rodhouse P.G. 2005. World squid resources. Review of the state of world marine fishery resources, FAO Tech. Rep. C2:175.

Ruiz-Cooley R.I., Ballance L.T., McCarthy M.D. 2013. Range Expansion of the Jumbo Squid in the NE Pacific: δ15N Decrypts Multiple Origins, Migration and Habitat Use. PloS One. 8(3): e59651. PMid:23527242 PMCid:PMC3601055

Sajina A.M., Chakraborty S.K., Jaiswar A.K., et al. 2011. Stock structure analysis of Megalaspis cordyla (Linnaeus, 1758) along the Indian coast based on truss network analysis. Fish. Res. 108: 100-105

Sánchez P. 1995. Age and growth of Illex coindetii. ICES J. Mar. Sci. 199: 441-444

Smale M.J., Clarke M.R., Klages N.T.W., et al. 1993. Octopod beak identification—resolution at a regional level (Cephalopoda, Octopoda: Southern Africa). S. Afr. J. Mar. Sci. 13(1): 269-293.

Uchikawa K., Sakai M., Wakabayashi T., et al. 2009. The relationship between paralarval feeding and morphological changes in the proboscis and beaks of the neon flying squid Ommastrephes bartramii. Fish. Sci. 75(2): 317-323.

Vega M.A., Rocha F.J., Guerra A., et al. 2002. Morphological difference between the Patagonian squid Loligo gahi populations from the Pacific and Atlantic Oceans. Bull. Mar. Sci. 71(2): 903-913

Villanueva R. 1992. Interannual growth differences in the oceanic squid Todarodes angolensis Adam in the northern Benguela upwelling system, based on statolith growth increment analysis. J. Exp. Mar. Biol. Ecol., 159(2): 157-177.

Wang Y.G., Chen X.J. 1998. The current exploitation of cephalopod resources in the world and the development of Chinese distant-water squid jigging fisheries. J. Shanghai Fish. Univ. 7: 285-287 (In Chinese with English abstract)

Wang Y.G., Chen X.J. 2005. The Resource and Biology of Economic Oceanic Squid in the World. Ocean Press, Beijing, pp. 79-295.

Wolff G.A. 1984. Identification and estimation of size from the beaks of 18 species of cephalopods from the Pacific Ocean. NOAA Technical Report NMFS 17: 1-50

Xavier J.C., Cherel Y. 2009. Cephalopod beak guide for the southern ocean. British Antarctic Survey Press, Cambridge, UK, 129 pp.

Xavier J.C., Clarke M.R., Magalhães M.C., et al. 2007. Current status of using beaks to identify cephalopods: III International Workshop and training course on Cephalopod beaks, Faial Island, Azores. Arquipélago 24: 41-48.

Xavier J.C., Phillips R.A., Cherel Y. 2011. Cephalopods in marine predator diet assessments: why identifying upper and lower beaks is important. ICES J. Mar. Sci. 68(9): 1857-1864.

Yatsu A. 2000. Age estimation of four oceanic squids, Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis, and Illex argentinus (Cephalopoda, Ommastrephidae) based on statolith Microstructure. Jpn. Agri. Res. Quart. 34: 75-80.

Yatsu A., Mori J. 2000. Early growth of the autumn cohort of neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean. Fish. Res. 45: 189-194.

Yatsu A., Midorikawa S., Shimada T., et al. 1997. Age and growth of the neon flying squid, Ommastrephes bartrami, in the North Pacific Ocean. Fish. Res. 29: 257-270

Yatsu A., Tanaka H., Mori J. 1998a. Population structure of the neon flying squid, Ommastrephes bartramii, in the North Pacific. In: Okutani T. (ed.), Contributed Papers to International Symposium on Large Pelagic Squids. Japan Marine Fisher Resources Research Center, Tokyo, pp. 31-48.

Yatsu A., Mochioka N., Morishita K., et al. 1998b. Strontium/calcium ratios in statoliths of the neon flying squid, Ommastrephes bartrami (Cephalopoda) in the North Pacific Ocean. Mar. Biol. 131: 275-282.

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