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Influence of temperature and salinity on the trace element incorporation into statoliths of the common cuttlefish (Sepia officinalis)

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Abstract

The use of statolith chemistry to trace migration pathways and distinguish populations of cephalopods is based on the assumption that the elemental composition of statoliths is influenced by physicochemical properties of the ambient environment. However, such influences have not been investigated experimentally up until now. This study presents the first microchemical analyses of cephalopod statoliths obtained from laboratory experiments under different controlled temperature and salinity conditions. Our results show that statolith chemical composition is strongly related to both salinity and temperature in ambient waters. The Ba/Ca ratio is negatively related to temperature and shows no relation to salinity. The I/Ca ratio is positively related to temperature and negatively to salinity. No Sr/Ca relation was found to either salinity or temperature, suggesting that the well-established proxy strontium is not as useful in cephalopod statoliths as in other biomineralized aragonites. Microanalysis of trace elements, however, shows an enormous potential for field studies on distribution, migration and stock separation of cephalopods. Furthermore, Synchrotron X-ray Fluorescence Analysis is introduced as a promising novel method for statolith analysis, providing a spatial resolution of typically 10–15 μm combined with detection limits down to 0.5 ppm.

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References

  • Allison N, Finch AA, Sutton SR, Newville M (2001) Strontium heterogeneity and speciation in coral aragonite: implications for the strontium paleothermometer. Geochim Cosmochim Acta 65(16):2669–2676

    Article  CAS  Google Scholar 

  • Arai T, Kotake A, Lokman PM, Miller MJ, Tsukamoto K (2004) Evidence of different habitat use by New Zealand freshwater eels Anguilla australis and A. dieffenbachii, as revealed by otolith microchemistry. Mar Ecol Prog Ser 266:213–225

    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 

  • Barrea RA, Pérez CA, Ramos AY, Sánchez HJ, Grenón M (2003) Distribution and incorporation of zinc in biological calcium phosphates. XRay Spectrom 32(5):387–395

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bath-Martin G, Thorrold SR, Jones CM (2004) Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus). Can J Fish Aquat Sci 61:34–42

    Article  Google Scholar 

  • Bettencourt V, Guerra A (2000) Growth increments and biomineralization process in cephalopod statoliths. J Exp Mar Biol Ecol 248:191–205

    Article  CAS  Google Scholar 

  • Bettencourt V, Guerra A (2001) Age studies based on daily growth increments in statoliths and growth lamellae in cuttlebone of cultured Sepia officinalis. Mar Biol 139:327–334

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

    Article  Google Scholar 

  • Clarke MR (1978) The cephalopod statolith—an introduction to its form. J Mar Biol Assoc UK 58:701–712

    Article  Google Scholar 

  • Denis V, Robin JP (2001) Present status of the French Atlantic fishery for cuttlefish (Sepia officinalis). Fish Res 52:11–22

    Article  Google Scholar 

  • Dietzel M, Gussone N, Eisenhauer A (2003) Co-precipitation of Sr2+ and Ba2+ with aragonite by membrane diffusion of CO2 between 10 and 50°C. Chem Geol 203:139–151

    Article  Google Scholar 

  • Durholtz MD, Lipinski MR, Przybylowicz WJ, Mesjasz-Przybylowicz J (1997) Nuclear microprobe mapping of statoliths of Chokka Squid Loligo vulgaris reynaudii d’Orbigny, 1845. Biol Bull 193:125–140

    Article  CAS  Google Scholar 

  • Elsdon TS, Gillanders BM (2002) Interactive effects of temperature and salinity on otolith chemistry: challenges for determining environmental histories of fish. Can J Fish Aquat Sci 59:1796–1808

    Article  CAS  Google Scholar 

  • Elsdon TS, Gillanders BM (2003) Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri. Mar Ecol Prog Ser 260:263–272

    Article  CAS  Google Scholar 

  • Espen PJ van, Nullens H, Adams F (1977) A computer analysis of X-ray fluorescence spectra. Nucl Instrum Methods 142:269–273

    Google Scholar 

  • FAO (2005) FISHSTAT plus global data set capture production 1950–2003 (FAO yearbook Fishery Statistics). ftp://www.ftp.fao.org/fi/stat/windows/fishplus/capdet.zip

  • Finch AA, Allison N, Sutton SR, Newville M (2003) Strontium in coral aragonite: characterization of Sr coordination by extended absorption X-ray fine structure. Geochim Cosmochim Acta 67(6):1197–1202

    Article  Google Scholar 

  • Gallahar NK, Kingsford MJ (1996) Factors influencing Sr/Ca ratios in otoliths of Girella elevata: an experimental investigation. J Fish Biol 48:174–186

    CAS  Google Scholar 

  • Greegor RB, Pingitore NE, Lytle FW (1997) Strontianite in coral skeletal aragonite. Science 275:1452–1454

    Article  CAS  Google Scholar 

  • Grieken RE van, Markowicz AA (1993) Handbook of X-ray spectrometry. Marcel Dekker, New York, Basel, Hongkong, p 704

    Google Scholar 

  • Hanlon RT, Bidwell JP, Tai R (1989) Strontium is required for statolith development and thus normal swimming behaviour of hatchling cephalopods. J Exp Biol 141(1):187–195

    CAS  PubMed  Google Scholar 

  • Hansteen TH, Sachs PM, Lechtenberg F (2000) Synchrotron-XRF microprobe analysis of silicate reference standards using fundamental-parameter quantification. Eur J Miner 12:25–31

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

    Article  CAS  Google Scholar 

  • Ikeda Y, Yatsu A, Arai N, Sakamoto W (2002a) 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, Okazaki J, Sakurai Y, Sakamoto W (2002b) Periodic variation in Sr/Ca ratios in statoliths of the Japanese Common Squid Todarodes pacificus Steenstrup, 1880 (Cephalopoda: Ommastrephidae) maintained under constant water temperature. J Exp Mar Biol Ecol 273(2):161-170

    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 

  • Jackson GD (1994) Application and future potential of statolith increment analysis in squid and sepioids. Can J Fish Aquat Sci 51:2612–2625

    Article  Google Scholar 

  • Kalish JM (1990) Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids. Fish Bull US 88:657–666

    Google Scholar 

  • Kristensen TK (1980) Periodical growth rings in cephalopod statoliths. Dana 1:39–51

    Google Scholar 

  • Knezovich JP (1994) Chemical and biological factors affecting bioavailability of contaminants in seawater. In: Hamelink JL, Landrum PF, Bergman HL, Benson WH (eds) Bioavailability: physical, chemical and biological interactions. Lewis Publishers, London, pp 23–30

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lechtenberg F, Garbe S, Bauch J, Dingwell DB, Freitag F, Haller M, Hansteen TH, Ippach P, Knöchel A, Radtke M, Romano C, Sachs PM, Schmincke HU, Ullrich HJ (1996) The X-ray fluorescence measurement place at beamline L of Hasylab. J Trace Microprobe Tech 14(3):561–587

    CAS  Google Scholar 

  • Limburg KE (1995) Otolith strontium traces environmental history of subyearling American shad Alosa sapidissima. Mar Ecol Prog Ser 119:25–5

    Article  Google Scholar 

  • Limburg KE (1996) Growth and migration of 0-year American shad (Alosa sapidissima) in the Hudson River estuary: otolith microstructural analysis. Can J Fish Aquat Sci 53:220–238

    Article  Google Scholar 

  • Limburg KE (1998) Anomalous migrations of anadromous herrings revealed with natural chemical tracers. Can J Fish Aquat Sci 55:431–437

    Article  Google Scholar 

  • Lipinski MR (1993) The deposition of statoliths: a working hypothesis. In: Okutani T, O’Dor RK, Kubodera T (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo

    Google Scholar 

  • Lipinski M, Przybylowicz WJ, Durholtz MD, Mesjasz-Przybylowicz J (1997) Quantitative micro-PIXE mapping of squid statoliths. Nucl Instrum Methods Phys Res B 130:374–380

    Article  CAS  Google Scholar 

  • Lowenstern JB (1993) Evidence for a copper-bearing fluid in magma erupted at the Valley of Ten-Thousand-Smokes, Alaska. Contrib Mineral Petrol 114:409–421

    Article  CAS  Google Scholar 

  • Martin RR, Naftel SJ, Machfie SM, Jones KW, Fenh H (2006) High variability of the metal content of tree growth rings as measured by synchrotron micro x-ray fluorescence spectrometry. X-Ray Spectrometry 35(1):52–56

    Article  Google Scholar 

  • Nakai I,Iwata R, Tsukamoto K (1999) Ecological study of the migration of eel by synchrotron radiation induced X-ray fluorescence imaging of otliths. Spectrochim Acta [B] 54(1):167–170

    Article  Google Scholar 

  • Radtke RL (1983) Chemical and structural characteristics of statoliths from the short-finned squid Illex illecebrosus. Mar Biol 76:47–54

    Article  CAS  Google Scholar 

  • Secor DH, Henderson-Arzapalo A, Piccoli PM (1995) Can otolith microchemistry chart patterns of migration and habitat utilization in anadromous fishes? J Exp Mar Biol Ecol 192:15–33

    Article  Google Scholar 

  • Secor DH, Rooker JR (2000) Is otolith strontium a useful scalar of life cycles in estuarine fishes? Fish Res 46(1):359–371

    Article  Google Scholar 

  • Shen CC, Lee T, Chen CY, Wang CH, Dai CF, Li LA (1996) The calibration of D[Sr/Ca] versus sea surface temperature relationship for Porites corals. Geochim Cosmochim Acta 60:3849–3858

    Article  CAS  Google Scholar 

  • Sholkovitz E, Shen GT (1995) The incorporation of rare earth elements in modern coral. Geochim Cosmochim Acta 59(13):2749–2756

    Article  CAS  Google Scholar 

  • Sohrin Y, Fujishima Y, Ueda K, Akiyama S, Mori K, Hasegawa H, Matsui M (1998) Dissolved niobium and tantalum in the North Pacific. Geophys Res Lett 25(7):999–1002

    Article  CAS  Google Scholar 

  • Smith SV, Buddermeier RW, Redalje RC, Houck JE (1979) Strontium-calcium thermometry in coral skeletons. Science 204:404–407

    Article  CAS  Google Scholar 

  • Thorn K, Cerrato RM, Rivers ML (1995) Elemental distributions in marine bivalve shells as measured by synchroton X-ray fluorescence. Biol Bull 188:57–67

    Article  CAS  Google Scholar 

  • Thorrold SR, Jones CM, Campana SE (1997) Response of otolith microchemistry to environmental variations experienced by larval and juvenile Atlantic croaker (Micropogonias undulatus). Limnol Oceanogr 42(1):102–111

    Article  CAS  Google Scholar 

  • Tsukamoto K, Nakai I, Tesch WV (1998) Do all freshwater eels migrate? Nature 396:635–636

    Article  CAS  Google Scholar 

  • Vincze L, Janssens K, Adams F (1993) A general Monte Carlo simulation of energy dipersive X-Ray fluourescence spectrometers-Part I. Spectrochim Acta 48B:553–573

    Article  CAS  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 

  • Zacherl DC, Paradis G, 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 

  • Zoeger N, Wobrauschek P, Streli C, Pepponi G, Roschger P, Falkenberg G, Osterode W (2005) Distribution of Pb and Zn in slices of human bone by synchrotron μ-XRF. X-Ray Spectrometry 43(2):140–143

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zumholz K, Klügel A, Hansteen TH, Piatkowski U (2007a) Statolith microchemistry traces environmental history of the boreoatlantic armhook squid Gonatus fabricii. Mar Ecol Progr Ser (in press)

  • Zumholz K, Hansteen TH, Hillion F, Horreard F, Piatkowski U (2007b) Elemental distribution in cephalopod statoliths: NanoSIMS provides new insights into nanoscale structure. Rev Fish Biol Fisher (in press)

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Acknowledgments

Thanks are due to Frank Lechtenberg for invaluable help with analytical and quantification procedures. Armelle Perrin and Juergen Beusen assisted in collecting Sepia eggs. The Kiel Aquarium team provided technical and logistical support during the experiments. This work was funded by the Deutsche Forschungsgemeinschaft (DFG PI 203/11-1, HA 2100/9-1, PI 203/11-2, PI 203-3).

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  1. Leibniz - Institute of Marine Sciences, IFM-GEOMAR, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Karsten Zumholz, Thor H. Hansteen, Uwe Piatkowski & Peter L. Croot

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  1. Karsten Zumholz
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  2. Thor H. Hansteen
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  3. Uwe Piatkowski
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Correspondence to Karsten Zumholz.

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Communicated by O. Kinne, Oldendorf/Luhe.

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Zumholz, K., Hansteen, T.H., Piatkowski, U. et al. Influence of temperature and salinity on the trace element incorporation into statoliths of the common cuttlefish (Sepia officinalis). Mar Biol 151, 1321–1330 (2007). https://doi.org/10.1007/s00227-006-0564-1

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