Abstract
Uroteuthis edulis is a widespread neritic cephalopod with a complex population structure and wide migration range. The life history of this species is still ambiguous. Statolith microchemistry is an effective indicator to reveal individual life history and migration route. In this study, the statolith microchemistry of U. edulis in different stocks was determined by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS), and the statolith diameter was clustered by using a multiple regression tree model (MRT) to analyze differences in the ratio of various elements to Ca at different life history stages. The analysis results showed that sodium (Na), magnesium (Mg), iron (Fe), strontium (Sr), and Barium (Ba) were the effective elements in four stocks. Five clusters were divided according to MRT and represented five ontogenetic stages. The Sr/Ca, Ba/Ca, and Mg/Ca ratios in summer and autumn stocks were significantly different from those of spring and winter stocks (P < 0.05). From the embryonic stage to sub-adult stage, the Sr/Ca ratio in spring and winter stocks was higher than those of summer and autumn stocks. The Sr/Ca ratio in spring, summer, and winter stocks were significantly different among different ontogenetic stages (P < 0.05). The Ba/Ca ratio in the four stocks were significantly different between larva and adults (P < 0.05). Therefore, the Sr/Ca and Ba/Ca ratios can be selected as the key indicators to speculate on the migration route of U. edulis. This study improves understanding of the statolith microchemistry differences among different stocks of U. edulis.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig4a_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig4b_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12562-023-01714-5/MediaObjects/12562_2023_1714_Fig5_HTML.png)
Similar content being viewed by others
References
Arbuckle NSM, Wormuth JH (2014) Trace elemental patterns in Humboldt squid statoliths from three geographic regions. Hydrobiologia 725:115–123. https://doi.org/10.1007/s10750-013-1608-4
Arkhipkin AI (2005) Statoliths as ‘black boxes’ (life recorders) in squid. Mar Freshwater Res 56:573–583. https://doi.org/10.1071/MF04158
Arkhipkin A, Campana SE, FitzGerald J, Thorrold SR (2004) Spatialand temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi). Can J Fish and Aquat Sci 61:1212–1224. https://doi.org/10.1139/F04-075
Chen XJ, Liu BL, Fang Z, Li JH (2019) Cephalopods. Ocean Press, Bei**g, pp 375–380 (in Chinese)
Chiang CI, Chung MT, Shiao JC, Wang PL, Chan TY, Yamaguchi A, Wang CH (2020) Seasonal movement patterns of the bigfin reef squid Sepioteuthis lessoniana predicted using statolith delta O-18 values. Front Mar Sci 7:249. https://doi.org/10.3389/fmars.2020.00249
Ching TY, Chen CS, Wang CH (2019) Spatiotemporal variations in life-history traits and statolith trace elements of Sepioteuthis lessoniana populations around northern Taiwan. J Mar Biol Assoc UK 99:203–213. https://doi.org/10.1017/S0025315417001801
Daryanani DS, Martino JC, Doubleday ZA (2021) Statolith chemistry: a new tool to understand the ecology and provenance of octopus. Rev Fish Biol Fisher 31:923–924. https://doi.org/10.1007/s11160-021-09671-x
Dauphin Y, Dufour E (2008) Nanostructures of the aragonitic otolith of cod (Gadus morhua). Micron 39:891–896. https://doi.org/10.1016/j.micron.2007.11.007
Durholtz MD, Lipinski MR, Przybylowicz WJ (1997) Nuclear microprobe map** of statoliths of chokka squid Loligo vulgaris reynaudii d’Orbigny. Biol Bull-Us 193:125–140. https://doi.org/10.2307/1542758
Fang Z (2016) Ecology of Neon Flying Squid Ommastrephes bartramii in North Pacific Ocean Based on Beak. Shanghai Ocean University, pp 103–117 (in Chinese)
Fang Z, Liu BL, Chen XJ, Chen Y (2019) Ontogenetic difference of beak elemental concentration and its possible application in migration reconstruction for Ommastrephes bartramii in the North Pacific Ocean. Acta Oceanol Sin 38:43–52. https://doi.org/10.1007/s13131-019-1431-5
Fang Z, ** Y, Chen XJ, Wang Y (2021) Differences in the concentrations of trace elements among different hard structures and their potential application in species identification: a case study on Loliginidae cryptic species. Mar Biol Res 17:350–361. https://doi.org/10.1080/17451000.2021.1957936
Gillanders BM, Wilkinson LM, Munro AR, Vries MC (2013) Statolith chemistry of two life history stages of cuttlefish: effects of temperature and seawater trace element concentration. Geochim Cosmochim Ac 101:12–33. https://doi.org/10.1016/j.gca.2012.10.005
Hoving HJT, Gilly WF, Markaida U, Benoit-Bird KJ, Brown ZW, Daniel P, Fieldk JC, Parassenti L, Liu BL, Campos B (2013) Extreme plasticity in life-history strategy allows a migratory predator (jumbo squid) to cope with a changing climate. Global Change Biol 19:2089–2103. https://doi.org/10.1111/gcb.12198
Hu GY (2016) Microstructure and microchemistry of beak for jumbo flying squid Dosdicus gigas off the Peruvian exclusive economic. Shanghai Ocean University, pp 77–118 (in Chinese)
Hu ZC, Gao S, Liu YS, Hu SH, Chen HH, Yuan HL (2008) Signal enhancement in laser ablation ICP-MS by addition of nitrogen in the central channel gas. J Anal Atom Spectrom 23:1093–1101. https://doi.org/10.1039/b804760j
Hu GY, Li JH, Liu BL, Liu N, Chen XJ (2021) Trophic ecology of Humboldt squid (Dosidicus gigas) in the oceanic waters off Ecuador: insight from isotopic signature analysis on beaks. Mar Freshwater Res 73:469–477. https://doi.org/10.1071/MF21183
** Y (2018) Fishery biology of Loliginidae in China Seas based on hard tissues. Shanghai Ocean University, pp 95–142 (in Chinese)
** Y, Li N, Yu J, Fang Z, Chen XJ (2021) Preliminary study on the migration characteristic of two loligo species in the northern South China Sea based on otolith microchemistry. Oceanol Et Limnol Sin 52:1540–1548. https://doi.org/10.11693/hyhz20210400080 (in Chinese)
Jones JB, Arkhipkin AI, Marriott AL, Pierce GJ (2019) Reprint of using statolith elemental signatures to confirm ontogenetic migrations of the squid Doryteuthis gahi around the Falkland Islands (Southwest Atlantic). Chem Geol 526:165–174. https://doi.org/10.1016/j.chemgeo.2018.04.002
Lacoue-Labarthe T, Reveillac E, Oberhansli F, Teyssie JL, Jeffree R, Gattuso JP (2011) Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris. Aquat Toxicol 105:166–176. https://doi.org/10.1016/j.aquatox.2011.05.021
Li N, Fang Z, Chen XJ (2020a) Fishery of swordtip squid Uroteuthis edulis: a review. J Dalian Ocean U 35:637–644. https://doi.org/10.16535/j.cnki,dlhyxb2019-208 (in Chinese)
Li N, Fang Z, Chen XJ (2020b) Fisheries biology characteristics of Uroteuthis rdulis off northern East China Sea. J Shanghai Ocean U 29:622–631. https://doi.org/10.12024/jsou.20190802774 (in Chinese)
Li N, Fang Z, Chen XJ, Feng ZP (2021a) Preliminary study on the migration characteristics of swordtip squid (Uroteuthis edulis) based on the trace elements of statolith in the East China Sea. Reg Stud Mar Sci 46:101879. https://doi.org/10.1016/j.rsma.2021.101879
Li N, Yu J, Fang Z, Chen XJ, Zhang Z (2021b) Age, growth and population structure of swordtip squid (Uroteuthis edulis) in the East China Sea based on statolith age information. J Fisher China 45:887–898. https://doi.org/10.11964/jfc.20200212154 (in Chinese)
Li N, Wang Y, Fang Z, Chen XJ, Feng ZP (2022) Relationships between daily growth of different groups of swordtip squid (Uroteuthis edulis) and environmental variables in the East China Sea. Acta Oceanol Sin 41:52–61. https://doi.org/10.1007/s13131-021-1905-0
Liu BL, Chen XJ, Chen Y, Qian WG (2011a) Trace elements in the statoliths of jumbo flying squid off the exclusive economic zones of Chile and Peru. Mar Ecol Prog Ser 429:93–101. https://doi.org/10.3354/meps09106
Liu BL, Chen XJ, Lu HJ, Ma J (2011b) Cephalopod statolith. Ocean Press Bei**g, pp 23–160 (in Chinese)
Liu BL, Chen XJ, Chen Y, Tian SQ (2013) Geographic variation in statolith trace elements of the Humboldt squid, Dosidicus gigas, in high seas of Eastern Pacific Ocean. Mar Biol 160:2853–2862. https://doi.org/10.1007/s00227-013-2276-7
Liu BL, Chen XJ, Fang Z, Hu S, Song Q (2015) A preliminary analysis of trace-elemental signatures in statoliths of different spawning cohorts for Dosidicus gigas off EEZ waters of Chile. J Ocean U China 14:1059–1067. https://doi.org/10.1007/s11802-015-2620-2
Liu BL, Cao J, Truesdell SB, Chen Y, Chen XJ, Tian SQ (2016) Reconstructing cephalopod migration with statolith elemental signatures: a case study using Dosidicus gigas. Fish Sci 82:425–433. https://doi.org/10.1007/s12562-016-0978-8
Liu Y, Wang XH, Du FY, Liu BL, Zhang P, Liu MN, Qiu YS (2019) Difference analysis of trace elements in statolith of Sthenoteuthis oualaniensis in South China Sea. South Fisher Sci China 15:15–24. https://doi.org/10.12131/20190039 (in Chinese)
Macy WK (1982) Development and application of an objective method for classifying long⁃finned squid, Loligo pealei, into sexual maturity stage. Fish B-NOAA 80:449–459
Martins RS, Roberts MJ, Vidal EAG, Moloney CL (2010) Effects of temperature on yolk utilization by chokka squid (Loligo reynaudii d’Orbigny, 1839) paralarvae. J Exp Mar Biol Ecol 386:19–26. https://doi.org/10.1016/j.jembe.2010.02.014
Natsukari Y, Nakanose T, Oda K (1988) Age and growth of loliginid squid Photololig edulis (Hoyle, 1885). J Exp Mar Biol Ecol 116:177–190. https://doi.org/10.1016/0022-0981(88)90054-8
Navarro MO, Bockmon EE, Frieder CA, Gonzalez JP, Levin LA (2014) Environmental pH, O-2 and capsular effects on the geochemical composition of statoliths of embryonic squid Doryteuthis opalescens. Water 6:2233–2254. https://doi.org/10.3390/w6082233
Pan XD, Zhang C, Ye ZJ, Xu BD, Li JC, Liu Y, Jiang T, Yang J, Tian YJ (2019) Trace elements in the otoliths of the Japanese Spanish mackerel (Scomberomorus niphonius) in the southern Yellow Sea. J Fisher China 43:907–916. https://doi.org/10.11964/jfc.20171111034 (in Chinese)
Pan XD, Ye ZJ, Xu BD, Jiang T, Yang J, Cheng JH, Tian YJ (2020) Combining otolith elemental signatures with multivariate analytical models to verify the migratory pattern of Japanese Spanish mackerel (Scomberomorus niphonius) in the southern Yellow Sea. Acta Oceanol Sin 39:54–64. https://doi.org/10.1007/s13131-020-1606-0
Pang YM, Tian YJ, Fu CH, Wang B, Li JC, Ren YP, Wan R (2018) Variability of coastal cephalopods in overexploited China Seas under climate change with implications on fisheries management. Fish Res 208:22–33. https://doi.org/10.1016/j.fishres.2018.07.004
Pang YM, Chen CS, Iwata Y (2020) Variations in female swordtip squid Uroteuthis edulis life history traits between southern Japan and northern Taiwan (Northwestern Pacific). Fisheries Sci 86:1005–1017. https://doi.org/10.1007/s12562-020-01465-7
Pecl GT, Jackson GD (2008) The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Rev Fish Biol Fisher 18:373–385. https://doi.org/10.1007/s11160-007-9077-3
Stooke-Vaughan GA, Obholzer ND, Baxendale S, Megason SG, Whitfield TT (2015) Otolith tethering in the zebrafish otic vesicle requires otogelin and alpha-tectorin. Development 142:1137–1145. https://doi.org/10.1242/dev.116632
Thomas ORB, Swearer SE (2019) Otolith biochemistry-a review. Rev Fish Sci Aquac 27:458–489. https://doi.org/10.1080/23308249.2019.1627285
Vidal EAG, Shea EK (2023) Cephalopod ontogeny and life cycle patterns. Front Mar Sci 10:1162735. https://doi.org/10.3389/fmars.2023.1162735
Vignon M (2015) Extracting environmental histories from sclerochronological structures - recursive partitioning as a mean to explore multi-elemental composition of fish otolith. Ecol Inform 30:159–169. https://doi.org/10.1016/j.ecoinf.2015.10.002
Wang KY (2009) Life history of Uroteuthis (Photololigo) edulis (Hoyle, 1885) in the Shelf Waters off Northeastern Taiwan. National Taiwan Ocean University, pp 22–47 (in Chinese)
Wang KY, Lee KT, Liao CH (2010) Age, growth and maturation of swordtip squid (Photololigo edulis) in the southern East China Sea. J Mar Sci Tech-Taiw 18:99–105. https://doi.org/10.1134/S0001433810010160
Wang KY, Chang KY, Liao CH, Lee MA, Lee KT (2013) Growth strategies of the swordtip squid, Uroteuthis Edulis, in response to environmental variations in the Southern East China Sea-a group analysis. B Mar Sci 89:677–698. https://doi.org/10.5343/bms.2012.1044
Wu R, Li JC, Zhang C, Pan XD, Jiang T, Yang J, Liu SD, Tian YJ (2021) Fine-scale variability in otolith chemistry: application to the life history analysis of Pacific cod (Gadus macrocephalus) in the Yellow Sea. Estuar Coast Shelf S 257:107392. https://doi.org/10.1016/j.ecss.2021.107392
Yamaguchi T, Kawakami Y, Matsuyama M (2015) Migratory routes of the swordtip squid Uroteuthis edulis inferred from statolith analysis. Aquat Biol 24:53–60. https://doi.org/10.3354/ab00635
Yamaguchi T, Aketagawa T, Miyamoto M, Hirose N, Matsuyama M (2018a) The use of statolith analyses and particle-tracking experiments to reveal the migratory route of the swordtip squid (Uroteuthis edulis) caught on the Pacific side of Japan. Fish Oceanogr 27:517–524. https://doi.org/10.1111/fog.12270
Yamaguchi T, Kawakami Y, Matsuyama M (2018b) Analysis of the hatching site and migratory behaviour of the swordtip squid (Uroteuthis edulis) caught in the Japan Sea and Tsushima Strait in autumn estimated by statolith analysis. Mar Biol Res 14:105–112. https://doi.org/10.1080/17451000.2017.1351616
Yamaguchi T, Aketagawa T, Takayama K, Hirose N, Matsuyama M (2019) Migratory routes of different sized swordtip squid (Uroteuthis edulis) caught in the Tsushima Strait. Fish Res 209:24–31. https://doi.org/10.1016/j.fishres.2018.08.008
Yamaguchi T, Takayama K, Hirose N, Matsuyama M (2020) Relationship between empirical water temperature and spring characteristics of swordtip squid (Uroteuthis edulis) caught in the eastern Tsushima Strait. Mar Biol Res 16:93–102. https://doi.org/10.1080/17451000.2020.1712420
Yatsu A, Mochioka N, Morishita K, Toh H (1998) Strontium:calcium ratios in statoliths of the neon flying squid, Ommastrephes bartrami (Cephalopoda), in the North Pacific Ocean. Mar Biol 131:275–282. https://doi.org/10.1007/s002270050320
Zhang K, Li M, Liu L, Liu Y, **ong W, Hu SH (2017) Correlation between microchemical characteristics of fish otolithes and water environment. Chem Bioeng 34:28–35. https://doi.org/10.3969/j.issn.1672-5425.2017.06.06 (in Chinese)
Zumholz K, Hansteen TH, Klugel A, Piatkowski U (2006) Food effects on statolith composition of the common cuttlefish (Sepia officinalis). Mar Biol 150:237–244. https://doi.org/10.1007/s00227-006-0342-0
Zumholz K, Klugel A, Hansteen T, Piatkowski U (2007) Statolith microchemistry traces the environmental history of the boreoatlantic armhook squid Gonatus fabricii. Mar Ecol Prog Ser 333:195–204. https://doi.org/10.3354/meps333195
Acknowledgements
The authors acknowledge the financial support from National Science Foundation of China (42306117), and Fund of Key Laboratory of Open-Sea Fishery Development, Ministry of Agriculture, P. R. China (LOF 2018-02). Moreover, the authors acknowledge the reviewers for their comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethical approval
Squid samples were randomly selected from fisheries catch taken by Chinese trawler fleets. Thus, the samples are part of the fisheries catch (with specimens being already dead when sampled). The samples were taken with permission from Shanghai Ocean University, which is in charge of oceanic fisheries research in China (Hu et al. 2021). The sampling protocol had been evaluated and approved by Shanghai Ocean University. The samples were taken strictly following the protocol. The sampled squid catch (dead squid) were frozen and then dissected in the laboratory. We confirm that the fisheries from which the squid were obtained were conducted by a legitimate Chinese company with appropriate permits to fish in the waters described in the paper. We also confirm that none of the squid was collected for the purpose of this study. They were caught as fisheries catch.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, N., Han, P., Chen, X. et al. Variation of statolith microchemistry among stocks of Uroteuthis edulis in the East China Sea. Fish Sci 89, 747–759 (2023). https://doi.org/10.1007/s12562-023-01714-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-023-01714-5