Skip to main content
SpringerLink
Log in

Geographic variation in statolith trace elements of the Humboldt squid, Dosidicus gigas, in high seas of Eastern Pacific Ocean

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We applied the solution-based inductively coupled plasma mass spectrometry to quantify trace elements in statoliths of Humboldt squid, Dosidicus gigas, collected from the high seas off Chile, Peru, and Costa Rica by Chinese squid jigging vessels during 2007–2009. All squid samples were aged and their spawning dates were back-calculated based on daily increments in statoliths. The most abundant trace elements in the whole statolith were Ca and Sr followed by other elements in the order of Fe, Mg, Zn, Ba, Cu, Mn, Ni, Al, Cr, Co, and U. Significant differences in Mn and Sr were found among samples from the three regions. Sr, Ni, Mn, and Co contributed significantly to the discrimination among the regions, with Co responsible for explaining most of the variation, followed by Ni, Mn, and Sr. Squid from the high seas off Costa Rica could be separated from those off Peru and Chile mostly due to the differences in Ni, Sr, and Co, while samples off Peru and Chile could be distinguished mainly because of differences in Mn and Co. Discriminant function analysis suggested that the overall cross-validated classification rate was 85.6 % with samples off Chile having the highest correct identification rates and samples off Costa Rica having the highest false classification rates. Significant positive relationships were found between sea surface temperature (SST) and Cr/Ca, Mn/Ca, and U/Ca, and there was a negative relationship between SST and Cu/Ca, Sr/Ca. This study suggests that the spatial difference in trace elements of statolith can be used to separate geographic populations of D. gigas and that elements having significant relationships with SST can be considered as natural indicators of ambient temperature.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arkhipkin AI (2005) Statolith as ‘black boxes’(life recorders) in squid. Mar Freshw Res 56:573–583

    Article  Google Scholar 

  • Arkhipkin AI, Campana SE, FitzGerald J, Thorrold SR (2004) Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi). Can J Fish Aquat Sci 61:1212–1224

    Article  Google Scholar 

  • Ashford JR, Jones CM, Hofman E, Everson I, Moreno C, Duhamel G, Villiams R (2005) Can otolith elemental signature record the capture site of Patagonian toothfish Dissostichus eleginoides, a fully marine fish in the southern ocean? Can J Fish Aquat Sci 62:2832–2840

    Article  CAS  Google Scholar 

  • Bath GE, Thorrold SR, Jones CM, Campana SE, McLaren JW, Lam JWH (2000) Sr and Ba uptake in aragonitic otolith of marine fish. Geochim Cosmochim Acta 64:1705–1714

    Article  CAS  Google Scholar 

  • Beck JW, Edwards RL, Ito E, Frederick W, Jacques R, Francis R, Pascale J, Christian H (1992) Sea-surface temperature from coral skeletal strontium/calcium ratios. Science 257:644–647

    Article  CAS  Google Scholar 

  • Becker BJ, Fodrie FJ, McMillan PA, Levin LA (2005) Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: a precursor to invertebrate larval tracking. Limnol Oceanogr 50:48–61

    Article  CAS  Google Scholar 

  • Begg GA, Cappo M, Cameron DS, Boyle S, Sellin MJ (1998) Stock discrimination of school mackerel, Scomberomorus queenslandicus, and spotted mackerel, Scomberomorus munroi, in coastal waters of eastern Australia by analysis of minor and trace elements in whole otoliths. Fish Bull 96:653–666

    Google Scholar 

  • Benites C, Valdivieso V (1986) Resultados de la pesca exploratoria de 1979/80 y desembarque de cefalópodos pelágicos en el litoral Peruano. Bol Inst Mar del Perú 10:107–139

    Google Scholar 

  • Bettencourt V, Guerra A (1999) Carbon- and oxygen-isotope composition of the cuttlebone of Sepia officinalis: a tool for predicting ecological information? Mar Biol 133:651–657

    Article  Google Scholar 

  • Bruland KW, Donat JR, Hutchins DA (1991) Interactive influences of bioactive trace metals on biological production in oceanic waters. Limnol Oceanogr 36:1555–1577

    Article  CAS  Google Scholar 

  • Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297

    Article  CAS  Google Scholar 

  • Campana SE, Gagne JA, McLaren JW (1995) Elemental fingerprinting of fish otoliths using ID-ICPMS. Mar Ecol Prog Ser 122:115–120

    Article  Google Scholar 

  • Campana SE, Chouinard GA, Hanson JM, Fréchet A, Brattey J (2000) Otolith elemental fingerprints as biological tracers of fish stocks. Fish Res 46:343–357

    Article  Google Scholar 

  • Chen XJ, Zhao XH (2005) Catch distribution of jumbo flying squid and its relationship with SST in the offshore waters of Chile. Mar Fish 27:173–176 (In Chinese with English Abstract)

    Google Scholar 

  • Chen XJ, Li JH, Liu BL, Chen Y, Li G, Fang Z, Tian SQ (2013) Age, growth and population structure of Jumbo flying squid, Dosidicus gigas, off the Costa Rica Dome. J Mar Biol Assoc UK 93:567–573

    Article  Google Scholar 

  • Cherel Y, Hobson K (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

    Article  Google Scholar 

  • Clarke R, Paliza O (2000) The Humboldt current squid Dosidicus gigas (Orbigny, 1835). Rev Biol Mar Oceanogr 35:1–38

    Google Scholar 

  • Correia AT, Pipa T, Gonçalves JMS, Erzini K, Hamer PA (2011) Insights into population structure of Diplodus vulgaris along the SW Portuguese coast from otolith elemental signatures. Fish Res 111:82–91

    Article  Google Scholar 

  • Dawe EG, Natsukari Y (1991) Light microscopy. In: Jereb P, Ragonese S, Boletzky SV (eds) Squid age determination using statoliths. Proceedings of the international workshop held in the Istituto di Tecnologia della Pesca e del Pescato, Special publication, pp 83–95

  • Doubleday ZA, Pecl GT, Semmens JM, Danyushevsky L (2008a) Stylet elemental signatures indicate population structure in a holobenthic octopus species, Octopus pallidus. Mar Ecol Prog Ser 371:1–10

    Article  CAS  Google Scholar 

  • Doubleday ZA, Pecl GT, Semmens JM, Danyushevsky L (2008b) Using stylet elemental signatures to determine the population structure of Octopus maorum. Mar Ecol Prog Ser 360:125–133

    Article  Google Scholar 

  • Hanlon RT, Bidwell JP, Tait R (1989) Strontium is required for statolith development and thus normal swimming behavior of hatching cephalopods. J Exp Biol 141:187–195

    CAS  Google Scholar 

  • Ichii T, Mahapatra K, Watanabe T, Yatsu A, Inagake D, Okada Y (2002) Occurrence of jumbo fying squid Dosidicus gigas aggregations associated with the countercurrent ridge off the Costa Rica Dome during 1997 El Niño and 1999 La Niña. Mar Ecol Prog Ser 231:151–166

    Article  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W (1995) Preliminary report on the PIXE analysis of the squid statoliths. Int J PIXE 5:159–162

    Article  CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Kidokoro H, Yoshida K (1996a) Relationship between statoliths and environmental variables in cephalopods. Int J PIXE 6:339–345

    Article  CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Nateewathana A, Murayama T, Yatsu A, Yoshida K (1996b) PIXE analysis of trace elements in squid statoliths: compositon between Ommastrephidae and Loliginidae. Int J PIXE 6:537–542

    Article  CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Kidokoro H, Yatsu A, Nateewathana A, Yoshida K (1997) Comparison on trace elements in squid statoliths of different species origin as available key for taxonomic and phylogenetic study. Int J PIXE 7:141–146

    Article  CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Kidokoro H, Yoshida K (1998) Microchemistry of the statoliths of the Japanese common squid Todarodes pacificus with special reference to it relation to the vertical temperature profiles of squid habitat. Fish Sci 64(2):179–184

    CAS  Google Scholar 

  • Ikeda Y, Arai N, Sakamoto W, Kidokoro H, Mitsuhashi M, Yoshida K (1999) Preliminary report on PIXE analysis for trace elements of Octopus dofleini statoliths. Fish Sci 65:161–162

    CAS  Google Scholar 

  • Ikeda Y, Yatsu A, Arai N, Sakamoto W (2002) Concentration of statolith trace elements in the jumbo flying squid during El Niño and non-El Niño years in the eastern Pacific. J Mar Biol Assoc UK 82:863–866

    Article  CAS  Google Scholar 

  • Ikeda Y, Arai N, Kidokoro H, Sakamoto W (2003) Strontium:calcium ratios in statoliths of Japanese common squid Todarodes pacificus (Cephalopoda: Ommastrephidae) as indicators of migratory behaviour. Mar Ecol Prog Ser 251:169–179

    Article  CAS  Google Scholar 

  • Lea DW, Shen GT, Boly EA (1989) Coralline barium records temporal variability in equatorial Pacific upwelling. Nat 340:373–376

    Article  CAS  Google Scholar 

  • Lipinski MR, Underhill LG (1995) Sexual maturation in squid: quantum or continuum. S Afr J Mar Sci 15:207–223

    Article  Google Scholar 

  • Liu BL, Chen XJ, Ma J, Qian WG (2010) Review of studies of the microchemical structure of cephalopod statoliths. J Fish China 34:316–321 (In Chinese with English Abstract)

    Google Scholar 

  • Liu BL, Chen XJ, Lu HJ, Qian WG (2011) Trace elements in the statoliths of jumbo flying squid off the exclusive economic zones of Chile and Peru. Mar Ecol Prog Ser 420:93–101

    Article  Google Scholar 

  • Lukeneder A, Harzhauser M, Müllegger S, Piller WE (2008) Stable isotopes (δ18O and δ13C) in Spirula shells from three major oceans indicate developmental changes paralleling depth distributions. Mar Biol 154:175–182

    Article  CAS  Google Scholar 

  • Ma J (2010) Statolith microstructure and microchemistry of the neon flying squid, Ommastrephes bartramii, in the Northwest Pacific Ocean. MS Thesis, Shanghai Ocean University, China, p 82 (In Chinese with English Abstract)

  • Morris CC (1991) Statocyst fluid composition and its effects on calcium carbonate precipitation in the squid Alloteuthis subulata (Lamarck, 1798): towards a model for biomineralization. Bull Mar Sci 49:379–388

    Google Scholar 

  • Nevárez-Martínez MO, Hernández-Herrera A, Morales-Bojórquez E, Balmori-Ramírez A, Cisneros-Mata MA, Morales-Azpeitia R (2000) Biomass and distribution of the jumbo squid (Dosidicus gigas; d’Orbigny, 1835) in the Gulf of California, Mexico. Fish Res 49:129–140

    Article  Google Scholar 

  • Nigmatullin C, Nesis KN, Arkhipkin AI (2001) A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fish Res 54:9–19

    Article  Google Scholar 

  • Nishimoto MM, Washburn L, Warner RR, Love MS, Paradis GL (2010) Otolith elemental signatures reflect residency in coastal water masses. Environ Biol Fish 89:341–356

    Article  Google Scholar 

  • Rocha F, Vega M (2003) Overview of cephalopod fisheries in Chilean waters. Fish Res 60:151–159

    Article  Google Scholar 

  • Rodhouse PG, Robinson K, Gajdatsy SB, Daly HI, Ashmore MJS (1994) Growth, age structure and environmental history in the cephalopod Martialia hyadei (Teuthoidea: Ommastrephidae) at the Atlantic Polar Frontal Zone and on the Patagonian Shelf Edge. Antarct Sci 6:259–267

    Google Scholar 

  • Rooker JR, Secor DH, Zdanowicz VS, Itoh T (2001) Discrimination of northern bluefin tuna from nursery areas in the Pacific Ocean using otolith chemistry. Mar Ecol Prog Ser 218:275–282

    Article  CAS  Google Scholar 

  • Sandoval-Castellanos E, Uribe-Alcocer M, Díaz-Jaimes P (2007) Population genetic structure of jumbo squid (Dosidicus gigas) evaluated by RAPD analysis. Fish Res 83:113–118

    Article  Google Scholar 

  • Shen GT, Dunbar RB (1995) Environmental controls on uranium in reef corals. Geochim Cosmochim Acta 59:2009–2024

    Article  CAS  Google Scholar 

  • Silva N, Rojas N, Fedele A (2009) Water masses in the Humboldt Current System: properties, distribution, and the nitrate deficit as a chemical water mass tracer for equatorial subsurface water off Chile. Deep-sea Res PT II 56:1004–1020

    Article  CAS  Google Scholar 

  • Staaf DJ, Ruiz-Cooley RI, Elliger C, Lebaric Z, Campos B, Markaida U, Gilly WF (2010) Ommastrephid squids Sthenoteuthis oualaniensis and Dosidicus gigas in the eastern Pacific show convergent biogeographic breaks but contrasting population structures. Mar Ecol Prog Ser 418:165–178

    Article  Google Scholar 

  • Swart PK, Elderfield H, Greaves MJ (2002) A high-resolution calibration of Sr/Ca thermometry using the Caribbean coral Montastraea annularis. Geochem Geophys Geosyst 3:1–11

    Article  Google Scholar 

  • Taipe A, Yamashiro C, Mariategui L, Rojas P, Roque C (2001) Distribution and concentrations of jumbo flying squid (Dosidicus gigas) off the Peruvian coast between 1991 and 1999. Fish Res 54:21–32

    Article  Google Scholar 

  • Waluda CM, Yamashiro C, Elvidge CD, Hobson VR, Rodhouse PG (2004) Quantifying light-fishing for Dosidicus gigas in the eastern Pacific using satellite remote sensing. Remote Sens Environ 91:129–133

    Article  Google Scholar 

  • Warner RR, Hamilton SL, Sheehy MS, Zeidberg LD, Brady BC, Caselle JE (2009) Geographic variation in natal and early larval trace-elemental signatures in the statoliths of the market squid Doryteuthis (formerly Loligo) opalescens. Mar Ecol Prog Ser 379:109–121

    Article  CAS  Google Scholar 

  • Yamane K, Shirai K, Nagakura Y, Yamaguchi M, Takiya A, Horii T, Tanaka N, Yamane S, Arai T, Otake T (2010) Spatial variation of otolith elemental compositions in Pacific herring Clupea pallasii. Aquat Biol 10:293–300

    Article  Google Scholar 

  • Yatsu A, Midorikawa S, Shimada T, Uozumi Y (1997) Age and growth of the neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean. Fish Res 29:257–270

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ye XC, Chen XJ (2007) Study of mantle length composition and maturity of jumbo flying squid (Dosidicus gigas) in fishing ground off Peru. J Shanghai Fish Univ 16(4):347–350 (In Chinese with English Abstract)

    CAS  Google Scholar 

  • Zacherl DC (2005) Spatial and temporal variation in statolith and protoconch trace elements as natural tags to track larval dispersal. Mar Ecol Prog Ser 290:145–163

    Article  CAS  Google Scholar 

  • Zacherl DC, Paradis GD, Lea DW (2003) Barium and strontium uptake into larval protoconchs and statoliths of the marine neogastropod Kelletia kelletii. Geochim Cosmochim Acta 67:4091–4099

    Article  CAS  Google Scholar 

  • Zumholz K, Hansteen TH, Klügel A, Piatkowski U (2006) Food effects on statolith compositon of the common cuttlefish (Sepia officinalis). Mar Biol 150:237–244

    Article  CAS  Google Scholar 

  • Zumholz K, Hansteen TH, Piatkowski U, Croot PL (2007a) Influence of temperature and salinity on the trace element incorporation into statoliths of the common cuttlefish (Sepia officinalis). Mar Biol 151:1321–1330

    Article  CAS  Google Scholar 

  • Zumholz K, Klügel A, Hansteen TH, Piatkowski U (2007b) Statolith microchemistry traces environmental history of the boreoatlantic armhook squid Gonatus fabricii. Mar Ecol Prog Ser 333:195–204

    Article  CAS  Google Scholar 

  • Zúñiga MJ, Cubillos LA, Ibáñez C (2008) A regular pattern of periodicity in the monthly catch of jumbo squid (Dosidicus gigas) along the Chilean coast (2002–2005). Cien Mar 34:91–99

    Google Scholar 

Download references

Acknowledgments

We appreciate the State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences for element analyses. This work was funded by National Science Foundation of China (NSFC41276156), State 863 projects (2012AA092303), the innovation Program of Shanghai Municipal Education Commission (13YE091), and Shanghai Leading Academic Discipline Project (Fisheries Discipline, Code A). Y. Chen was supported by Shanghai Oversea Teaching Scholar Program and SHOU International Center for Marine Sciences.

Author information

Authors and Affiliations

  1. College of Marine Sciences, Shanghai Ocean University, Hucheng Ring Road 999, Lingang New City, Shanghai, 201306, China

    Bilin Liu, Xinjun Chen, Yong Chen & Siquan Tian

  2. The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, 999 Hucheng Ring Road, Shanghai, 201306, China

    Bilin Liu, Xinjun Chen, Yong Chen & Siquan Tian

  3. School of Marine Sciences, University of Maine, Orono, ME, 04469, USA

    Yong Chen

  4. International Center for Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China

    Yong Chen

Authors
  1. Bilin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xinjun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siquan Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xinjun Chen.

Additional information

Communicated by U. Sommer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, B., Chen, X., Chen, Y. et al. Geographic variation in statolith trace elements of the Humboldt squid, Dosidicus gigas, in high seas of Eastern Pacific Ocean. Mar Biol 160, 2853–2862 (2013). https://doi.org/10.1007/s00227-013-2276-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2276-7

Keywords

Search

Navigation