Ontogenetic difference of beak elemental concentration and its possible application in migration reconstruction for Ommastrephes bartramii in the North Pacific Ocean

  • Zhou Fang
  • Bilin Liu
  • Xinjun ChenEmail author
  • Yong Chen


The migration route of oceanic squid provides critical information for us to understand their spatial and temporal variations. Mark-recapture and electronic tags tend to be problematic during processing. Cephalopod hard structures such as the beak, containing abundant ecological information with stable morphology and statolith-like sequences of growth increments, may provide information for studying spatio-temporal distribution. In this study, we developed a method, which is based on elemental concentration of beaks at different ontogenetic stages and sampling locations, to reconstruct the squid migration route. We applied this method to Ommastrephes bartramii in the North Pacific Ocean. Nine trace elements were detected in the rostrum sagittal sections (RSS) of the beak using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). For those elements, significant differences were found between the different ontogenetic stages for phosphorus (P), copper (Cu) and zinc (Zn). Sodium (Na), P and Zn were chosen as indicators of sea surface temperature (SST) and a regression model was estimated. The high probability of occurrence in a particular area represented the possible optimal squid location based on a Bayesian model. A reconstructed migration route in this study, combining all the locations at different ontogenetic stages, was consistent with that hypothesized in previous studies. This study demonstrates that the beak can provide useful information for identifying the migration routes of oceanic squid.


Ommastrephes bartramii beak trace element ontogenetic stage migration route 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



The support of the scientific surveys by commercial jigging vessel F/V Jinhai 827 is gratefully acknowledged.


  1. Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6): 716–723, doi: CrossRefGoogle Scholar
  2. Alabia I D, Saitoh S I, Hirawake T, et al. 2016. Elucidating the potential squid habitat responses in the central North Pacific to the recent ENSO flavors. Hydrobiologia, 772(1): 215–227, doi: CrossRefGoogle Scholar
  3. Alabia I D, Saitoh S I, Mugo R, et al. 2015. Seasonal potential fishing ground prediction of neon flying squid (Ommastrephes bartramii) in the western and central North Pacific. Fisheries Oceanography, 24(2): 190–203, doi: CrossRefGoogle Scholar
  4. Arbuckle N S M, Wormuth J H. 2014. Trace elemental patterns in Humboldt squid statoliths from three geographic regions. Hydrobiologia, 725(1): 115–123, doi: CrossRefGoogle Scholar
  5. Arkhipkin A I. 2005. Statoliths as ‘black boxes’(life recorders) in squid. Marine and Freshwater Research, 56(5): 573–583, doi: CrossRefGoogle Scholar
  6. Arkhipkin A I, Shcherbich Z N. 2012. Thirty years’ progress in age determination of squid using statoliths. Journal of the Marine Biological Association of the United Kingdom, 92(6): 1389–1398, doi: CrossRefGoogle Scholar
  7. Bettencourt V, Guerra A. 2000. Growth increments and biomineralization process in cephalopod statoliths. Journal of Experimental Marine Biology and Ecology, 248(2): 191–205, doi: CrossRefGoogle Scholar
  8. Bower J R, Ichii T. 2005. The red flying squid (Ommastrephes bartramii): a review of recent research and the fishery in Japan. Fisheries Research, 76(1): 39–55, doi: CrossRefGoogle Scholar
  9. Boyle P, Rodhouse P G. 2005. Cephalopods. Ecology and Fisheries. Oxford: Blackwell Publishing, 222–233CrossRefGoogle Scholar
  10. Chen Xinjun, Liu Bilin, Chen Yong. 2008. A review of the development of Chinese distant-water squid jigging fisheries. Fisheries Research, 89(3): 211–221, doi: CrossRefGoogle Scholar
  11. Chen Xinjun, Lu Huajie, Liu Bilin, et al. 2012. Species identification of Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis and Illex argentines (Ommastrephidae) using beak morphological variables. Scientia Marina, 76(3): 473–481, doi: CrossRefGoogle Scholar
  12. Elsdon T, Gillanders B. 2005. Strontium incorporation into calcified structures: separating the effects of ambient water concentration and exposure time. Marine Ecology Progress Series, 285: 233–243, doi: CrossRefGoogle Scholar
  13. Fang Zhou, Liu Bilin, Chen Xinjun, et al. 2016a. Sexual asynchrony in the development of beak pigmentation for the neon flying squid Ommastrephes bartramii in the North Pacific Ocean. Fisheries Science, 82(5): 737–746, doi: CrossRefGoogle Scholar
  14. Fang Zhou, Li Jianhua, Thompson K, et al. 2016b. Age, growth, and population structure of the red flying squid (Ommastrephes bartramii) in the North Pacific Ocean, determined from beak microstructure. Fishery Bulletin, 114(1): 34–44, doi: 10.7755/FBCrossRefGoogle Scholar
  15. Fang Zhou, Thompson K, Jin Yue, et al. 2016c. Preliminary analysis of beak stable isotopes (δ 13C and δ 15N) stock variation of neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean. Fisheries Research, 177: 153–163, doi: CrossRefGoogle Scholar
  16. Franco-Santos R M, Vidal E A G. 2014. Beak development of early squid paralarvae (Cephalopoda: Teuthoidea) may reflect an adaptation to a specialized feeding mode. Hydrobiologia, 725(1): 85–103, doi: CrossRefGoogle Scholar
  17. Hernández-López J L, Castro-Hernández J L, Hernández-Garcia V. 2001. Age determined from the daily deposition of concentric rings on common octopus (Octopus vulgaris) beaks. Fishery Bulletin, 99(4): 679–684Google Scholar
  18. 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. Fisheries Oceanography, 13(5): 295–309, doi: CrossRefGoogle Scholar
  19. 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. Marine Ecology Progress Series, 378: 1–11, doi: CrossRefGoogle Scholar
  20. Igarashi H, Ichii T, Sakai M, et al. 2017. Possible link between interannual variation of neon flying squid (Ommastrephes bartramii) abundance in the North Pacific and the climate phase shift in 1998/1999. Progress in Oceanography, 150: 20–34, doi: CrossRefGoogle Scholar
  21. 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. Marine Ecology Progress Series, 251: 169–179, doi: CrossRefGoogle Scholar
  22. 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(3–4): 141–146CrossRefGoogle Scholar
  23. Ikeda Y, Yatsu A, Arai N, et al. 2002. Concentration of statolith trace elements in the jumbo flying squid during El Nino and non-El Niño years in the eastern Pacific. Journal of the Marine Biological Association of the UK, 82(5): 863–866, doi: CrossRefGoogle Scholar
  24. Jennings S, Cogan S M. 2015. Nitrogen and carbon stable isotope variation in northeast Atlantic fishes and squids. Ecology, 96(9): 2568, doi: CrossRefGoogle Scholar
  25. Jereb P, Roper C F E. 2010. Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. In: Myopsid and Oegopsid Squids. Vol. 2. Rome: FAO Species Catalogue for Fishery Purposes, 269Google Scholar
  26. Kato Y, Sakai M, Mmasujima M, et al. 2014. Effects of hydrographic conditions on the transport of neon flying squid Ommastrephes bartramii larvae in the North Pacific Ocean. Hidrobiológica, 24(1): 33–38Google Scholar
  27. Liu Bilin, Cao Jie, Truesdell S B, et al. 2016. Reconstructing cephalopod migration with statolith elemental signatures: a case study using Dosidicus gigas. Fisheries Science, 82(3): 425–433, doi: CrossRefGoogle Scholar
  28. Liu Bilin, Chen Xinjun, Chen Yong, et al. 2013. Geographic variation in statolith trace elements of the Humboldt squid, Dosidicus gigas, in high seas of Eastern Pacific Ocean. Marine Biology, 160(11): 2853–2862, doi: CrossRefGoogle Scholar
  29. Liu Bilin, Chen Yong, Chen Xinjun. 2015a. Spatial difference in elemental signatures within early ontogenetic statolith for identifying Jumbo flying squid natal origins. Fisheries Oceanography, 24(4): 335–346, doi: CrossRefGoogle Scholar
  30. Liu Bilin, Chen Xinjun, Chen Yong, et al. 2015c. Determination of squid age using upper beak rostrum sections: technique improvement and comparison with the statolith. Marine Biology, 162(8): 1685–1693, doi: CrossRefGoogle Scholar
  31. Liu Bilin, Fang Zhou, Chen Xinjun, et al. 2015b. Spatial variations in beak structure to identify potentially geographic populations of Dosidicus gigas in the Eastern Pacific Ocean. Fisheries Research, 164: 185–192, doi: CrossRefGoogle Scholar
  32. Mereu M, Agus B, Cannas R, et al. 2015. Mark-recapture investigation on Octopus vulgaris specimens in an area of the central western Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom, 95(1): 131–138, doi: CrossRefGoogle Scholar
  33. Miserez A, Li Youli, Waite J H, et al. 2007. Jumbo squid beaks: inspiration for design of robust organic composites. Acta Biomaterialia, 3(1): 139–149, doi: CrossRefGoogle Scholar
  34. Miserez A, Schneberk T, Sun Chengjun, et al. 2008. The transition from stiff to compliant materials in squid beaks. Science, 319(5871): 1816–1819, doi: CrossRefGoogle Scholar
  35. Miserez A, Rubin D, Waite J H. 2010. Cross-linking chemistry of squid beak. Journal of Biological Chemistry, 285(49): 38115–38124, doi: CrossRefGoogle Scholar
  36. Moltschaniwskyj N, Cappo M. 2009. Alternatives to sectioned otoliths: the use of other structures and chemical techniques to estimate age and growth for marine vertebrates and invertebrates. In: Green B S, Mapstone B D, Carlos G, et al, eds. Tropical Fish Otoliths: Information for Assessment, Management and Ecology. Dordrecht: Springer, 133–173CrossRefGoogle Scholar
  37. Murata M, Nakamura Y. 1998. Seasonal migration and diel vertical migration of the neon flying squid, Ommastrephes bartramii, in the North Pacific. In: Okutani T, ed. Contributed Papers to International Symposium on Large Pelagic Squids. Tokyo: Japan Marine Fishery Resources Research Center, 13–30Google Scholar
  38. Navarro J, Coll M, Somes C, et al. 2013. Trophic niche of squids: Insights from isotopic data in marine systems worldwide. Deep Sea Research Part II: Topical Studies in Oceanography, 95: 93–102, doi: CrossRefGoogle Scholar
  39. Nishikawa H, Igarashi H, Ishikawa Y, et al. 2014. Impact of paralarvae and juveniles feeding environment on the neon flying squid (Ommastrephes bartramii) winter-spring cohort stock. Fisheries Oceanography, 23(4): 289–303, doi: CrossRefGoogle Scholar
  40. Nishikawa H, Toyoda T, Masuda S, et al. 2015. Wind-induced stock variation of the neon flying squid (Ommastrephes bartramii) winter-spring cohort in the subtropical North Pacific Ocean. Fisheries Oceanography, 24(3): 229–241, doi: CrossRefGoogle Scholar
  41. O’Dor R K, Balch N. 1985. Properties of iIlex illecebrosus egg masses potentially influencing larval oceanographic distribution. NAFO Science Council Studies, 9: 69–76Google Scholar
  42. Perales-Raya C, Almansa E, Bartolomé A, et al. 2014b. Age validation in Octopus vulgaris beaks across the full ontogenetic range: beaks as recorders of life events in octopuses. Journal of Shellfish Research, 33(2): 481–493, doi: CrossRefGoogle Scholar
  43. Perales-Raya C, Bartolomé A, García-Santamaría M T, et al. 2010. Age estimation obtained from analysis of octopus (Octopus vulgaris Cuvier, 1797) beaks: Improvements and comparisons. Fisheries Research, 106(2): 171–176, doi: CrossRefGoogle Scholar
  44. Perales-Raya C, Jurado-Ruzafa A, Bartolomé A, et al. 2014a. Age of spent Octopus vulgaris and stress mark analysis using beaks of wild individuals. Hydrobiologia, 725(1): 105–114, doi: CrossRefGoogle Scholar
  45. R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Google Scholar
  46. Ripley B, Ribeiro P J, Diggle P J. 2001. Spatial Statistics in R and geoR: A Package for Geostatistical Analysis. Analysis, 6(1): 14–15Google Scholar
  47. Rodríguez-Navarro A, Guerra A, Romanek C S, et al. 2006. Life history of the giant squid Architeuthis as revealed from stable isotope and trace elements signatures recorded in its beak. In: Moltschaniwskyj N, ed. Cephalopod Life Cycle. Cephalopod International Advisory Council Symposium 2006 (CIAC’ 06). 6–10 February 2006, Hotel Grand Chancellor, Hobart, Tasmania, 97Google Scholar
  48. Semmens J M, Pecl G T, Gillanders B M, et al. 2007. Approaches to resolving cephalopod movement and migration patterns. Reviews in Fish Biology and Fisheries, 17(2–3): 401–423, doi: CrossRefGoogle Scholar
  49. Sims D W, Genner M J, Southward A J, et al. 2001. Timing of squid migration reflects North Atlantic climate variability. Proceedings of the Royal Society B: Biological Sciences, 268(1485): 2607–2611, doi: CrossRefGoogle Scholar
  50. Slominski A, Tobin D J, Shibahara S, et al. 2004. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiological Reviews, 84(4): 1155–1228, doi: CrossRefGoogle Scholar
  51. Staaf D J, Coop S C, Haddock S H, et al. 2008. Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae. Journal of the Marine Biological Association of the UK, 88(4): 759–770CrossRefGoogle Scholar
  52. Swan G A. 1974. Structure, chemistry, and biosynthesis of the melanins. In: Herz W, Grisebach H, Kirby G W, eds. Fortschritte der Chemie Organischer Naturstoffe/Progress in the Chemistry of Organic Natural Products. Vienna: Springer, 521–582CrossRefGoogle Scholar
  53. Tanaka H. 2001. Tracking the neon flying squid by the biotelemetry system, in the central North Pacific Ocean. Aquabiology (in Japanese), 23(6): 533–539Google Scholar
  54. Tian Siquan, Chen Xinjun, Chen Yong, et al. 2009. Evaluating habitat suitability indices derived from CPUE and fishing effort data for Ommatrephes bratramii in the Northwestern Pacific Ocean. Fisheries Research, 95(2–3): 181–188, doi: CrossRefGoogle Scholar
  55. Tian Yongjun, Nashida K, Sakaji H. 2013. Synchrony in the abundance trend of spear squid Loligo bleekeri in the Japan Sea and the Pacific Ocean with special reference to the latitudinal differences in response to the climate regime shift. ICES Journal of Marine Science, 70(5): 968–979, doi: CrossRefGoogle Scholar
  56. VanBogelen R A, Olson E R, Wanner B L, et al. 1996. Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. Journal of Bacteriology, 178(15): 4344–4366, doi: CrossRefGoogle Scholar
  57. Venables W N, Ripley B D. 2002. Modern Applied Statistics with S. 4th ed. New York: SpringerCrossRefGoogle Scholar
  58. Vijai D, Sakai M, Wakabayashi T, et al. 2015. Effects of temperature on embryonic development and paralarval behavior of the neon flying squid Ommastrephes bartramii. Marine Ecology Progress Series, 529: 145–158, doi: CrossRefGoogle Scholar
  59. Watanabe H, Kubodera T, Ichii T, et al. 2004. Feeding habits of neon flying squid Ommastrephes bartramii in the transitional region of the central North Pacific. Marine Ecology Progress Series, 266: 173–184, doi: CrossRefGoogle Scholar
  60. Watanabe H, Kubodera T, Ichii T, et al. 2008. Diet and sexual maturation of the neon flying squid Ommastrephes bartramii during autumn and spring in the Kuroshio-Oyashio transition region. Journal of the Marine Biological Association of the United Kingdom, 88: 381–389CrossRefGoogle Scholar
  61. Wearmouth V J, Durkin O C, Bloor I S M, et al. 2013. A method for long-term electronic tagging and tracking of juvenile and adult European common cuttlefish Sepia officinalis. Journal of Experimental Marine Biology and Ecology, 447: 149–155, doi: CrossRefGoogle Scholar
  62. Young R E, Harman R F. 1988. “Larva”, “paralarva” and “subadult” in cephalopod terminology. Malacologia, 29(1): 201–207Google Scholar
  63. Zumholz K. 2005. The influence of environmental factors on the micro-chemical composition of cephalopod statoliths [dissertation]. Kiel: University of KielGoogle Scholar

Copyright information

© Chinese Society for Oceanography and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zhou Fang
    • 1
    • 3
    • 4
    • 5
  • Bilin Liu
    • 1
    • 3
    • 4
    • 5
  • Xinjun Chen
    • 1
    • 2
    • 3
    • 4
    • 5
    Email author
  • Yong Chen
    • 6
  1. 1.College of Marine SciencesShanghai Ocean UniversityShanghaiChina
  2. 2.Laboratory for Marine Fisheries Science and Food Production ProcessesPilot National Laboratory for Marine Science and Technology (Qingdao)QingdaoChina
  3. 3.National Engineering Research Center for Oceanic FisheriesShanghai Ocean UniversityShanghaiChina
  4. 4.Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources of Ministry of EducationShanghai Ocean UniversityShanghaiChina
  5. 5.Key Laboratory of Oceanic Fisheries ExplorationMinistry of AgricultureShanghaiChina
  6. 6.School of Marine SciencesUniversity of MaineOronoUSA

Personalised recommendations