Advertisement

Analytical and Bioanalytical Chemistry

, Volume 399, Issue 6, pp 2175–2184 | Cite as

Temperature dependency of element incorporation into European eel (Anguilla anguilla) otoliths

  • Lasse Marohn
  • Volker Hilge
  • Karsten Zumholz
  • Andreas Klügel
  • Heike Anders
  • Reinhold Hanel
Original Paper

Abstract

The present study experimentally tested the influence of water temperature on the inclusion of 15 elements into juvenile European eel (Anguilla anguilla) otoliths in freshwater. It should be investigated (1) if temperature effects on otolith Sr/Ca might impair the interpretation of migration studies and (2) if the elemental composition of otoliths can be used to reconstruct experienced temperature histories of eels. Therefore, eels were kept under full experimental conditions at three different water temperatures (14 °C, 19 °C and 24 °C) for 105 days. Thereafter, laser ablation inductively coupled mass spectrometry (LA-ICPMS) was conducted on the outer edge of their otoliths. Our analyses revealed significant temperature effects on otolith Na/Ca, Sr/Ca, Mg/Ca, Mn/Ca, Ba/Ca, Zr/Ca and Y/Ca ratios. Variations of Sr/Ca caused by temperature were far below those used to detect eel movements between waters of different salinities and will therefore not affect the interpretation of migration studies. Elemental fingerprints of Sr/Ca, Mg/Ca, Mn/Ca and Ba/Ca ratios resulted in clearly separated groups according to temperature treatments, indicating that changes in water temperature might lead to characteristic changes in otolith element composition. However, the successful application of elemental fingerprints to reconstruct moderate changes of water temperature seems doubtful because the influence of somatic growth on otolith microchemistry still remains unclear, and temperature-induced variations could be overlaid by changes of water element concentrations during growth periods. Nevertheless, our results contribute to the completion of knowledge about factors influencing element incorporation and help to explain variations in element composition of fish otoliths.

Figure

Juvenile European eels (Anguilla anguilla)

Keywords

Anguilla anguilla Otolith Microchemistry LA-ICPMS Temperature effect 

Notes

Acknowledgements

We thank one anonymous reviewer for his helpful comments. Andreas Drahotta is acknowledged for the construction and maintenance of the rearing system, the daily feeding of eels and his invaluable help during Alizarin marking. We also thank Nina Bergmann for statistical advice, Festus Nashima for his help during otolith preparation and Andrea Frommel for proofreading. This study was funded by the German Federal Ministry of Consumer Protection, Food and Agriculture (BMELV) through the project “Habitat selection of the European eel” (04HS065).

References

  1. 1.
    Radtke RL, Kinzie RA, Folsom SD (1988) Age at recruitment of Hawaiian fresh-water gobies. Environ Biol Fish 23:205–213CrossRefGoogle Scholar
  2. 2.
    Halden NM, Babaluk JA, Campbell JL, Teesdale WJ (1995) Scanning proton microprobe analysis of strontium in an arctic charr, Salvelinus alpinus, otolith—implications for the interpretation of anadromy. Environ Biol Fish 43:333–339CrossRefGoogle Scholar
  3. 3.
    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 192:15–33CrossRefGoogle Scholar
  4. 4.
    Tzeng WN, Severin KP, Wickstrom H (1997) Use of otolith microchemistry to investigate the environmental history of European eel Anguilla anguilla. Mar Ecol Prog Ser 149:73–81CrossRefGoogle Scholar
  5. 5.
    Edmonds JS, Moran MJ, Caputi N, Morita M (1989) Trace-element analysis of fish sagittae as an aid to stock identification—pink snapper (Chrysophrys auratus) in Western Australian waters. Can J Fish Aquat Sci 46:50–54CrossRefGoogle Scholar
  6. 6.
    Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297CrossRefGoogle Scholar
  7. 7.
    Gillanders BM, Kingsford MJ (2000) Elemental fingerprints of otoliths of fish may distinguish estuarine ‘nursery’ habitats. Mar Ecol Prog Ser 201:273–286CrossRefGoogle Scholar
  8. 8.
    Rooker JR, Secor DH, Zdanowicz VS, De Metrio G, Relini LO (2003) Identification of Atlantic bluefin tuna (Thunnus thynnus) stocks from putative nurseries using otolith chemistry. Fish Oceanogr 12:75–84CrossRefGoogle Scholar
  9. 9.
    Kalish JM (1989) Otolith microchemistry—validation of the effects of physiology, age and environment on otolith composition. J Exp Mar Biol Ecol 132:151–178CrossRefGoogle Scholar
  10. 10.
    Kalish JM (1992) Formation of a stress-induced chemical check in fish otoliths. J Exp Mar Biol Ecol 162:265–277CrossRefGoogle Scholar
  11. 11.
    Otake T, Ishii T, Ishii T, Nakahara M, Nakamura R (1997) Changes in otolith strontium: calcium ratios in metamorphosing Conger Myriaster leptocephali. Mar Biol 128:565–572CrossRefGoogle Scholar
  12. 12.
    Tzeng WN, Shiao JC, Iizuka Y (2002) Use of otolith Sr:Ca ratios to study the riverine migratory behaviors of Japanese eel Anguilla japonica. Mar Ecol Prog Ser 245:213–221CrossRefGoogle Scholar
  13. 13.
    Kalish JM (1990) Use of otolith microchemistry to distinguish the progeny of sympatric anadromous and non-anadromous salmonids. Fish B-NOAA 88:657–666Google Scholar
  14. 14.
    Tzeng WN (1996) Effects of salinity and ontogenetic movements on strontium:calcium ratios in the otoliths of the Japanese eel, Anguilla japonica Temminck and Schlegel. J Exp Mar Biol Ecol 199:111–122CrossRefGoogle Scholar
  15. 15.
    Bath GE, Thorrold SR, Jones CM, Campana SE, McLaren JW, Lam JWH (2000) Strontium and barium uptake in aragonitic otoliths of marine fish. Geochim Cosmochim Acta 64:1705–1714CrossRefGoogle Scholar
  16. 16.
    Elsdon TS, Gillanders BM (2006) Temporal variability in strontium, calcium, barium, and manganese in estuaries: implications for reconstructing environmental histories of fish from chemicals in calcified structures. Estuar Coast Shelf Sci 66:147–156CrossRefGoogle Scholar
  17. 17.
    Hamer PA, Jenkins GP (2007) Comparison of spatial variation in otolith chemistry of two fish species and relationships with water chemistry and otolith growth. J Fish Biol 71:1035–1055CrossRefGoogle Scholar
  18. 18.
    Elsdon TS, Wells BK, Campana SE, Gillanders BM, Jones CM, Limburg KE, Secor DH, Thorrold SR, Walther BD (2008) Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanogr Mar Biol 46:297–330CrossRefGoogle Scholar
  19. 19.
    Payan P, De Pontual H, Boeuf G, Mayer-Gostan N (2004) Endolymph chemistry and otolith growth in fish. C R Palevol 3:535–547CrossRefGoogle Scholar
  20. 20.
    Hoff GR, Fuiman LA (1993) Morphometry and composition of red drum otoliths—changes associated with temperature, somatic growth-rate, and age. Comp Biochem Physiol A 106:209–219CrossRefGoogle Scholar
  21. 21.
    Otake T, Ishii T, Nakahara M, Nakamura R (1994) Drastic changes in otolith strontium/calcium ratios in leptocephali and glass eels of Japanese eel Anguilla japonica. Mar Ecol Prog Ser 112:189–193CrossRefGoogle Scholar
  22. 22.
    Tzeng WN, Chang CW, Wang CH, Shiao JC, Iizuka Y, Yang YJ, You CF, Lozys L (2007) Misidentification of the migratory history of anguillid eels by Sr/Ca ratios of vaterite otoliths. Mar Ecol Prog Ser 348:285–295CrossRefGoogle Scholar
  23. 23.
    Limburg KE (1995) Otolith strontium traces environmental history of subyearling American Shad Alosa sapidissima. Mar Ecol Prog Ser 119:25–35CrossRefGoogle Scholar
  24. 24.
    Farrell J, Campana SE (1996) Regulation of calcium and strontium deposition on the otoliths of juvenile tilapia, Oreochromis niloticus. Comp Biochem Physiol A 115:103–109CrossRefGoogle Scholar
  25. 25.
    Buckel JA, Sharack BL, Zdanowicz VS (2004) Effect of diet on otolith composition in Pomatomus saltatrix, an estuarine piscivore. J Fish Biol 64:1469–1484CrossRefGoogle Scholar
  26. 26.
    Sadovy Y, Severin KP (1992) Trace-elements in biogenic aragonite—correlation of body growth-rate and strontium levels in the otoliths of the white grunt, Haemulon plumieri (Pisces, Haemulidae). B Mar Sci 50:237–257Google Scholar
  27. 27.
    Sadovy Y, Severin KP (1994) Elemental patterns in red hind (Epinephelus guttatus) otoliths from Bermuda and Puerto-Rico reflect growth-rate, not temperature. Can J Fish Aquat Sci 51:133–141CrossRefGoogle Scholar
  28. 28.
    Radtke RL (1989) Strontium calcium-concentration ratios in fish otoliths as environmental indicators. Comp Biochem Physiol A 92:189–193CrossRefGoogle Scholar
  29. 29.
    Townsend DW, Radtke RL, Corwin S, Libby DA (1992) Strontium-calcium ratios in juvenile atlantic herring Clupea harengus L otoliths as a function of water temperature. J Exp Mar Biol Ecol 160:131–140CrossRefGoogle Scholar
  30. 30.
    Hoff GR, Fuiman LA (1995) Environmentally-induced variation in elemental composition of red drum (Sciaenops ocellatus) otoliths. B Mar Sci 56:578–591Google Scholar
  31. 31.
    Tsukamoto K, Nakai I, Tesch WV (1998) Do all freshwater eels migrate? Nature 396:635–636CrossRefGoogle Scholar
  32. 32.
    Jessop BM, Shiao JC, Iizuka Y, Tzeng WN (2002) Migratory behaviour and habitat use by American eels Anguilla rostrata as revealed by otolith microchemistry. Mar Ecol Prog Ser 233:217–229CrossRefGoogle Scholar
  33. 33.
    Limburg KE, Wickström H, Svedäng H, Elfman M, Kristiansson P (2003) Do stocked freshwater eels migrate? Evidence from the baltic suggests “yes”. Am Fish S S 33:275–284Google Scholar
  34. 34.
    Arai T, Hirata T (2006) Differences in the trace element deposition in otoliths between marine- and freshwater-resident Japanese eels, Anguilla japonica, as determined by laser ablation ICPMS. Environ Biol Fish 75:173–182CrossRefGoogle Scholar
  35. 35.
    Daverat F, Limburg KE, Thibault I, Shiao JC, Dodson JJ, Caron FO, Tzeng WN, Iizuka Y, Wickstrom H (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla, A-japonica and A-rostrata. Mar Ecol Prog Ser 308:231–241CrossRefGoogle Scholar
  36. 36.
    Marohn L, Prigge E, Zumholz K, Klugel A, Anders H, Hanel R (2009) Dietary effects on multi-element composition of European eel (Anguilla anguilla) otoliths. Mar Biol 156:927–933CrossRefGoogle Scholar
  37. 37.
    Kawakami Y, Mochioka N, Morishita K, Tajima T, Nakagawa H, Toh H, Nakazono A (1998) Factors influencing otolith strontium/calcium ratios in Anguilla japonica elvers. Environ Biol Fish 52:299–303CrossRefGoogle Scholar
  38. 38.
    Tzeng WN (1994) Temperature effects on the incorporation of strontium in otolith of Japanese eel Anguilla japonica. J Fish Biol 45:1055–1066CrossRefGoogle Scholar
  39. 39.
    Dekker W, Casselman JM, Cairns DK, Tsukamoto K, Jellyman D, Lickers H et al (2003) Québec declaration of concern—worldwide decline of eel resources necessitates immediate action. Fisheries 28:28–30Google Scholar
  40. 40.
    ICES (2009) Report of the 2009 session of the joint EIFAC/ICES working group on eels. 7–12 Sep 2009, Gothenburg. Available at http://www.ices.dk/reports/ACOM/2009/WGEEL/WGEELfinalReport2009.pdf
  41. 41.
    Martin GB, Thorrold SR, Jones CM (2004) Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus). Can J Fish Aquat Sci 61:34–42CrossRefGoogle Scholar
  42. 42.
    Simon J, Dörner H (2005) Marking the European eel with oxytetracycline, alizarin red and coded wire tags: an evaluation of methods. J Fish Biol 67:1486–1491CrossRefGoogle Scholar
  43. 43.
    Pearce NJG, Perkins WT, Westgate JA, Gorton MP, Jackson SE, Neal CL, Chenery SP (1997) A compilation of new and published major and trace element data for NIST SRM 610 and NIST SRM 612 glass reference materials. Geostand Newsl 21:115–144CrossRefGoogle Scholar
  44. 44.
    Gao S, Liu X, Yuan H, Hattendorf B, Günther D, Chen L, Hu W (2002) Determination of forty-two major and trace elements in USGS and NIST SRM glasses by laser ablation-inductively coupled plasma-mass spectrometry. Geostand Newsl 26:181–196CrossRefGoogle Scholar
  45. 45.
    Yoshinaga J, Nakama A, Morita M, Edmonds JS (2000) Fish otolith reference material for quality assurance of chemical analyses. Mar Chem 69:91–97CrossRefGoogle Scholar
  46. 46.
    Neukamm R (2009) Final report, FIAF Pilotprojekt zur Förderung des Aales in den Gewässersystemen Nord-Ostsee-Kanal und Elbe-Lübeck-Kanal. Available at http://www.lsfv-sh.de/downloads/sonstiges/fiaf-aalprojekt-abschlussbericht-2006-2008/view.html
  47. 47.
    Campana SE (1983) Calcium deposition and otolith check formation during periods of stress in coho salmon, Oncorhynchus kisutch. Camp Biochem Physiol 75A:215–220Google Scholar
  48. 48.
    Payan P, De Pontual H, Edeyer A, Borelli G, Boeuf G, Mayer-Gostan N (2004) Effects of stress on plasma homeostasis, endolymph chemistry, and check formation during otolith growth in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1247–1255CrossRefGoogle Scholar
  49. 49.
    Shiao JC, Lozys L, Iizuka Y, Tzeng WN (2006) Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr:Ca ratios. J Fish Biol 69:749–769CrossRefGoogle Scholar
  50. 50.
    Elsdon TS, Gillanders BM (2004) Fish otolith chemistry influenced by exposure to multiple environmental variables. J Exp Mar Biol Ecol 313:269–284CrossRefGoogle Scholar
  51. 51.
    Gallahar NK, Kingsford MJ (1996) Factors influencing Sr/Ca ratios in otoliths of Girella elevata: an experimental investigation. J Fish Biol 48:174–186Google Scholar
  52. 52.
    Chesney EJ, McKee BM, Blanchard T, Chan LH (1998) Chemistry of otoliths from juvenile menhaden Brevoortia patronus: evaluating strontium, strontium:calcium and strontium isotope ratios as environmental indicators. Mar Ecol Prog Ser 171:261–273CrossRefGoogle Scholar
  53. 53.
    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 59:1796–1808CrossRefGoogle Scholar
  54. 54.
    Yamashita Y, Otake T, Yamada H (2000) Relative contributions from exposed inshore and estuarine nursery grounds to the recruitment of stone flounder, Platichthys bicoloratus, estimated using otolith Sr:Ca ratios. Fish Oceanogr 9:316–327CrossRefGoogle Scholar
  55. 55.
    Kraus RT, Secor DH (2004) Incorporation of strontium into otoliths of an estuarine fish. J Exp Mar Biol Ecol 302:85–106CrossRefGoogle Scholar
  56. 56.
    Tzeng WN, Severin KP, Wickstrom H, Wang CH (1999) Strontium bands in relation to age marks in otoliths of European eel Anguilla anguilla. Zool Stud 38:452–457Google Scholar
  57. 57.
    Miller JA (2009) The effects of temperature and water concentration on the otolith incorporation of barium and manganese in black rockfish Sebastes melanops. J Fish Biol 75:39–60CrossRefGoogle Scholar
  58. 58.
    Martin GB, Thorrold SR (2005) Temperature and salinity effects on magnesium, manganese, and barium incorporation in otoliths of larval and early juvenile spot Leiostomus xanthurus. Mar Ecol Prog Ser 293:223–232CrossRefGoogle Scholar
  59. 59.
    Martin GB, Wuenschel MJ (2006) Effect of temperature and salinity on otolith element incorporation in juvenile gray snapper Lutjanus griseus. Mar Ecol Prog Ser 324:229–239CrossRefGoogle Scholar
  60. 60.
    Elsdon TS, Gillanders BM (2003) Reconstructing migratory patterns of fish based on environmental influences on otolith chemistry. Rev Fish Biol Fish 13:219–235Google Scholar
  61. 61.
    Walther BD, Thorrold SR (2006) Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Mar Ecol Prog Ser 311:125–130CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Lasse Marohn
    • 1
  • Volker Hilge
    • 2
  • Karsten Zumholz
    • 3
  • Andreas Klügel
    • 4
  • Heike Anders
    • 4
  • Reinhold Hanel
    • 2
  1. 1.Leibniz-Institute of Marine Sciences, IFM-GEOMARKielGermany
  2. 2.Johann Heinrich von Thünen-Institut, Federal Research Institute for Rural Areas, Forestry and FisheriesInstitute for Fisheries EcologyHamburgGermany
  3. 3.Berufsbildungszentrum am Nord-OstseekanalRendsburgGermany
  4. 4.Department of GeosciencesUniversity of BremenBremenGermany

Personalised recommendations