Advertisement

Age interpretation in eulachon (Thaleichthys pacificus) as suggested by otolith microchemical signatures

  • Irina M. BensonEmail author
  • Craig R. Kastelle
  • Thomas E. Helser
  • Jonathan A. Short
  • Delsa M. Anderl
Article

Abstract

Eulachon (Thaleichthys pacificus) are forage fish that play an important role in the ecosystem as prey for many species. Given their continuing population decline, determining accurate ages is necessary for age-structured stock assessments. This study employed microchemistry analysis to identify group differences and help interpret growth zone patterns on otolith surfaces. Specimens were collected off the coast of Oregon, in the coastal areas of Southeast Alaska, and in the southeastern Bering Sea. Laser-ablation inductively-coupled plasma mass spectrometry (LA-ICP-MS) was used to measure elemental ratios in the otoliths along a continuous track from the core to the proximoventral margin. Ba:Ca, Sr:Ca, Zn:Ca, and Mg:Ca signatures suggested that eulachon specimens from three geographic regions are different based on their elemental profiles. For the Oregon specimens, fluctuations in Ba:Ca and Zn:Ca signatures appeared consistent with otolith growth zones and most likely were the result of seasonal coastal upwelling events. Variations in Ba:Ca and Zn:Ca were useful as annual markers for eulachon otoliths from the Bering Sea. For the Southeast Alaska specimens, analysis of the Ba:Ca and Zn:Ca oscillations was not straightforward. Further work is needed to understand the link between otolith microchemistry, fish physiology, and regional environmental factors.

Keywords

Eulachon Otoliths Trace elements Forage fish Microchemistry Age determination 

Notes

Acknowledgments

We express sincere appreciation to everyone whose contributions made this research successful. The ABL staff who collected and processed the Southwestern Alaska samples: JJ Vollenweider and David Clausen collected the samples, Chris Kondzela curated the sample collections, and Wei Cheng and Molly Krehlik extracted the otoliths. ODFW staff who donated Oregon samples and offered advice: Bob Hannah, Josie Thompson, and Lisa Kautzi. Adrian Clarke (UNBC) gave advice during conception of the study. Betty Goetz (AFSC) shared her scientific insight and expertise on otolith ageing. Beth Matta (AFSC) offered advice during the course of this research, including design of the study, elemental data post-processing, and review of the manuscript. Jessica Miller and Andy Ungerer (OSU W.M.Keck Collaboratory) provided assistance with LA-ICPMS analysis. Kimberly Rand, Matt Wilson, and Andy Whitehouse (AFSC) offered their suggestions for the manuscript improvement. The Age and Growth Program staff (AFSC) participated in discussion during various stages of this study. The findings and conclusions in the paper are those of the authors and do not necessarily represent the views of the National Marine Fisheries Service, NOAA.

References

  1. Bath GE, Thorrold SR, Jones CM, Campana SE, McLaren JW, Lam JW (2000) Strontium and barium uptake in aragonitic otoliths of marine fish. Geochim Cosmochim Acta 64:1705–1714CrossRefGoogle Scholar
  2. Box GEP, Cox DR (1964) An analysis of transformations. JR Stat Soc, B:211–252Google Scholar
  3. Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297CrossRefGoogle Scholar
  4. Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242CrossRefGoogle Scholar
  5. Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032CrossRefGoogle Scholar
  6. Campana SE, Thorrold SR (2001) Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38CrossRefGoogle Scholar
  7. Campana SE, Thorrold SR, Jones CM, Günther D, Tubrett M, Longerich H, Jackson S, Halden NM, Kalish JM, Piccoli P, Pontual H de, Troadec H, Panfili J, Secor DH, Severin KP, Sie SH, Thresher R, Teesdale WJ, Campbell JL (1997) Comparison of accuracy, precision, and sensitivity in elemental assays of fish otoliths using the electron microprobe, proton-induced X-ray emission, and laser ablation inductively coupled plasma mass spectrometry. Can J Fish Aquat Sci 54:2068–2079Google Scholar
  8. Carroll J, Falkner KK, Brown ET, Moore WS (1993) The role of the Ganges-Brahmaputra mixing zone in supplying barium and 226Ra to the Bay of Bengal. Geochim Cosmochim Acta 57:2981–2990CrossRefGoogle Scholar
  9. Chan LH, Drummond D, Edmond JM, Grant B (1977) On the barium data from the Atlantic GEOSECS expedition. Deep-Sea Res 24:613–649CrossRefGoogle Scholar
  10. Chan P, Halfar J, Williams B, Hetzinger S, Steneck R, Zack T, Jacob DE (2011) Freshening of the Alaska coastal current recorded by coralline algal Ba/Ca ratios. J Geophys Res 116:1–8CrossRefGoogle Scholar
  11. Chang M-Y, Geffen AJ (2013) Taxonomic and geographic influences on fish otolith microchemistry. Fish Fish 14:458–492CrossRefGoogle Scholar
  12. Clarke AD, Lewis A, Telmer KH, Shrimpton JM (2007) Life history and age at maturity of an anadromous smelt, the eulachon Thaleichthys pacificus (Richardson). J Fish Biol 71:1479–1493CrossRefGoogle Scholar
  13. Coffey M, Dehairs F, Collette O, Luther G, Church T, Jickells T (1997) The behaviour of dissolved barium in estuaries. Estuar Coast Shelf Sci 45:113–121CrossRefGoogle Scholar
  14. Ducklow HW, Schofield O, Vernet M, Stammerjohn S, Erickson M (2012) Multiscale control of bacterial production by phytoplankton dynamics and sea ice along the western Antarctic Peninsula: a regional and decadal investigation. J Mar Syst 98-99:26–39CrossRefGoogle Scholar
  15. Falkner KK, Macdonald RW, Carmack EC, Weingartner T (1994) The potential of barium as a tracer of Arctic water masses. In: Johannessen OM, Muench RD, Overland JE (eds) The polar oceans and their role in shaping the global environment: the Nansen centennial volume / O. M. Johannessen, R. D. Muench, J. E. Overland, editors: Am Geophys Union:63–76Google Scholar
  16. Flannery BG, Wenburg JK, Lewis CJ, Norcross BL, Spangler RE (2009) Genetic population structure of Alaska eulachon. Alaska fish. Tech. Rep. 106, US Fish Wildl Serv:1–22Google Scholar
  17. Fowler AJ (1990) Validation of annual growth increments in the otoliths of a small, tropical coral reef fish. Mar Ecol Prog Ser 64:25–38CrossRefGoogle Scholar
  18. Fowler AJ, Gillanders BM, Hall KC (2005) Relationship between elemental concentration and age from otoliths of adult snapper (Pagrus auratus Sparidae): implications for movement and stock structure. Mar Freshw Res 56:661CrossRefGoogle Scholar
  19. Guay CK, Falkner KK (1998) A survey of dissolved barium in the estuaries of major Arctic rivers and adjacent seas. Cont Shelf Res 18:859–882CrossRefGoogle Scholar
  20. Gustafson RG, Ford MJ, Adams PB, Drake JS, Emmett RL, Fresh KL, Rowse M, Spangler EAK, Spangler RE, Teel DJ, Wilson MT (2012) Conservation status of eulachon in the California current. Fish Fish 13:121–138CrossRefGoogle Scholar
  21. Gustafson R, Lee YW, Ward E, Somers K, Tuttle V, Jannot J (2016) Status review update of eulachon (Thaleichthys pacificus) listed under the Endangered Species Act: southern distinct population segment. 25 March 2016 Report to NMFS–WCR from NFSCGoogle Scholar
  22. Halden NM, Mejia SR, Babaluk JA, Reist JD, Kristofferson AH, Campbell JL, Teesdale WJ (2000) Oscillatory zinc distribution in Arctic char (Salvelinus alpinus) otoliths. Fish Res 46:289–298CrossRefGoogle Scholar
  23. Hannah RW, Jones SA, Lomeli MJ, Wakefield WW (2011) Trawl net modifications to reduce the bycatch of eulachon (Thaleichthys pacificus) in the ocean shrimp (Pandalus jordani) fishery. Fish Res 110:277–282CrossRefGoogle Scholar
  24. Hanson KC, Ostrand KG (2013) Evaluation of transmitter application techniques for use in research of adult eulachon. N Am J Fish Manag 33:1119–1124CrossRefGoogle Scholar
  25. Hay D, McCarter PB (2000) Status of the eulachon Thaleichthys pacificus in Canada. Canadian Stock Assessment Secretariat Research Document. 2000/145. Fish Oceans CanGoogle Scholar
  26. Hermann AJ, Stabeno PJ, Haidvogel DB, Musgrave DL (2002) A regional tidal/subtidal circulation model of the southeastern Bering Sea: development, sensitivity analyses and hindcasting. Deep-Sea Res II 49:5945–5967CrossRefGoogle Scholar
  27. Høie H, Folkvord A (2006) Estimating the timing of growth rings in Atlantic cod otoliths using stable oxygen isotopes. J Fish Biol 68(3):826–837CrossRefGoogle Scholar
  28. Hüssy K, Mosegaard H (2004) Atlantic cod (Gadus morhua) growth and otolith accretion characteristics modelled in a bioenergetics context. Can J Fish Aquat Sci 61:1021–1031CrossRefGoogle Scholar
  29. Hüssy K, Gröger J, Heidemann F, Hinrichsen H-H, Marohn L (2016) Slave to the rhythm: seasonal signals in otolith microchemistry reveal age of eastern Baltic cod (Gadus morhua). ICES J Mar Sci 73(4):1019–1032CrossRefGoogle Scholar
  30. Jochum KP, Weis U, Stoll B, Kuzmin D, Yang Q, Raczek I, Jacob DE, Stracke A, Birbaum K, Frick DA, Günther D, Enzweiler J (2011) Determination of reference values for NIST SRM 610-617 glasses following ISO guidelines. Geostand Geoanal Res 35:397–429CrossRefGoogle Scholar
  31. Kalish JM (1991) Determinants of otolith chemistry seasonal variation in the composition of blood plasma, endolymph and otoliths of bearded rock cod Pseudophycis barbatus. Mar Ecol Prog Ser 74:137–159CrossRefGoogle Scholar
  32. Kastelle CR, Helser TE, McKay JL, Jonhnston CG, Anderl DM, Matta ME, Nichol DG (2017) Age validation of Pacific cod (Gadus macrocephalus) using high-resolution stable oxygen isotope (δ18O) chronologies in otoliths. Fish Res 185:43–53CrossRefGoogle Scholar
  33. Kent A, Ungerer C (2006) Analysis of light lithophile elements (Li, Be, B) by laser ablation ICP-MS: comparison between magnetic sector and quadrupole ICP-MS. Am Mineral 91:1401–1411CrossRefGoogle Scholar
  34. Ladd C (2014) Seasonal and interannual variability of the Bering slope current. Deep-Sea Res II 109:5–13CrossRefGoogle Scholar
  35. Ladd C, Stabeno PJ (2012) Stratification on the Eastern Bering Sea shelf revisited. Deep-Sea Res II 65-70:72–83CrossRefGoogle Scholar
  36. Limburg KE, Wuenschel MJ, Hüssy K, Heimbrand Y, Samson M (2018) Making the otolith magnesium chemical calendar-clock tick: plausible mechanism and empirical evidence. Rev Fish Sci Aquaculture 26(4):479–493CrossRefGoogle Scholar
  37. Matta ME, Miller JA, Short JA, Helser TE, Hurst TP, Rand KM, Ormseth OA (2017) Spatial and temporal variation in otolith elemental signatures of age-0 Gulf of Alaska Pacific cod (Gadus macrocephalus). Deep Sea Res II (In Press).  https://doi.org/10.1016/j.dsr2.2017.08.015
  38. McCarter PB, Hay DE (1999) Distribution of spawning eulachon stocks in the central coast of British Columbia as indicated by larval surveys. Can Stock Assess Secret Res Doc 99:177Google Scholar
  39. Miller JA (2007) Scales of variation in otolith elemental chemistry of juvenile staghorn sculpin (Leptocottus armatus) in three Pacific Northwest estuaries. Mar Biol 151:483–494CrossRefGoogle Scholar
  40. Miller JA (2011) Effects of water temperature and barium concentration on otolith composition along a salinity gradient: implications for migratory reconstructions. J Exp Mar Biol Ecol 405:42–52CrossRefGoogle Scholar
  41. Miller JA, Banks MA, Gomez-Uchida D, Shanks AL (2005) A comparison of population structure in black rockfish (Sebastes melanops) as determined with otolith microchemistry and microsatellite DNA. Can J Fish Aquat Sci 62:2189–2198CrossRefGoogle Scholar
  42. Miller MB, Clough AM, Batson JN, Vachet RW (2006) Transition metal binding to cod otolith proteins. J Exp Mar Biol Ecol 329:135–143CrossRefGoogle Scholar
  43. Morales-Nin B, Swan SC, Gordon JDM, Palmer M, Geffen AJ, Shimmield T, Sawyer T (2005) Age-related trends in otolith chemistry of Merluccius merluccius from the North-Eastern Atlantic Ocean and the western Mediterranean Sea. Mar Freshw Res 56:599CrossRefGoogle Scholar
  44. Ormseth OA (2014) Appendix 2. Forage species report for the Gulf of Alaska. Plan Team for the Groundfish Fisheries of the Gulf of Alaska (compiler), Stock assessment and fishery evaluation report for the groundfish resources of the Gulf of Alaska: 1001–1039Google Scholar
  45. Ormseth OA (2015) Appendix Status of forage species in the Bering Sea and Aleutian Islands region. Plan Team for the Groundfish Fisheries of the Bering Sea and Aleutian Islands (compiler), Stock assessment and fishery evaluation report for the groundfish resources of the Bering Sea/Aleutian Islands regions: 1225–1270Google Scholar
  46. Pearce NJ, Perkins WT, Westgate JA, Gorton MP, Jackson SE, Neal CR, 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 Newslett 21:115–144CrossRefGoogle Scholar
  47. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, AustriaGoogle Scholar
  48. Ranaldi MM, Gagnon MM (2008) Trace metal incorporation in otoliths of black bream (Acanthopagrus butcheri Munro), an indicator of exposure to metal contamination. Water Air Soil Pollut 194:31–43CrossRefGoogle Scholar
  49. Schumacher JD, Kinder TH, Pashinski DJ, Charnell RL (1979) A structural front over the continental shelf of the eastern Bering Sea. J Phys Oceanogr 9:79–87CrossRefGoogle Scholar
  50. Smith WD, Miller JA, Heppell SS (2013) Elemental markers in elasmobranchs: effects of environmental history and growth on vertebral chemistry. PLoS ONE 8:e62423CrossRefGoogle Scholar
  51. Springer AM, McRoy CP, Flint MV (1996) The Bering Sea green belt: shelf-edge processes and ecosystem production. Fish Oceanogr 5:205–223CrossRefGoogle Scholar
  52. Stabeno P, Schumacher J, Ohtani K (1999) The physical oceanography of the Bering Sea. In: Loughlin T, Ohtani K (eds) Dynamics of the Bering Sea, pp 1–28Google Scholar
  53. Stabeno P, Bond N, Hermann A, Kachel N, Mordy C, Overland J (2004) Meteorology and oceanography of the Northern Gulf of Alaska. Cont Shelf Res 24:859–897CrossRefGoogle Scholar
  54. Stabeno P, Napp J, Mordy C, Whitledge T (2010) Factors influencing physical structure and lower trophic levels of the eastern Bering Sea shelf in 2005: sea ice, tides and winds. Prog Oceanogr 85:180–196CrossRefGoogle Scholar
  55. Stabeno PJ, Farley EV Jr, Kachel NB, Moore S, Mordy CW, Napp JM, Overland JE, Pinchuk AI, Sigler MF (2012) A comparison of the physics of the northern and southern shelves of the eastern Bering Sea and some implications for the ecosystem. Deep-Sea Res II 65-70:14–30CrossRefGoogle Scholar
  56. Stauffer G (2004) NOAA protocols for groundfish bottom trawl surveys of the nation’s fishery resources. NOAA Tech Memo. NMFS-F/SPO-65Google Scholar
  57. Sturrock AM, Trueman CN, Darnaude AM, Hunter E (2012) Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? J Fish Biol 81:766–795CrossRefGoogle Scholar
  58. Sturrock AM, Trueman CN, Milton JA, Waring CP, Cooper MJ, Hunter E (2014) Physiological influences can outweigh environmental signals in otolith microchemistry research. Mar Ecol Prog Ser 500:245–264CrossRefGoogle Scholar
  59. Sturrock AM, Hunter E, Milton JA, Johnson RC, Waring CP, Trueman CN, Leder E (2015) Quantifying physiological influences on otolith microchemistry. Methods Ecol Evol 6:806–816CrossRefGoogle Scholar
  60. Tabachnick BG, Fidell LS (1996) Using multivariate statistics, 3rd edn. Harper Collins College Publishers, New YorkGoogle Scholar
  61. Taylor JR (2003) Quantitative considerations of dissolved barium as a tracer in the Arctic Ocean. J Geophys Res 108Google Scholar
  62. Vancoppenolle M, Meiners KM, Michel C, Bopp L, Brabant F, Carnat G, Delille B, Lannuzel D, Madec G, Moreau S, Tison JL, van der Merwe P (2013) Role of sea ice in global biogeochemical cycles: emerging views and challenges. Quat Sci Rev 79:207–230CrossRefGoogle Scholar
  63. Vollenweider JJ, Heintz RA, Schaufler L, Bradshaw R (2011) Seasonal cycles in whole-body proximate composition and energy content of forage fish vary with water depth. Mar Biol 158:413–427CrossRefGoogle Scholar
  64. Wang S, Bailey D, Lindsay K, Moore JK, Holland M (2014) Impact of sea ice on the marine iron cycle and phytoplankton productivity. Biogeosciences 11:4713–4731CrossRefGoogle Scholar
  65. Washington Dept of Fish and Wildlife and Oregon Dept of Fish and Wildlife (2001) Washington and Oregon eulachon management plan. In: Washington Dept of fish and wildlifeGoogle Scholar
  66. Weingartner TJ, Danielson SL, Royer TC (2005) Freshwater variability and predictability in the Alaska coastal current. Deep-Sea Res II 52:169–191CrossRefGoogle Scholar
  67. Weingartner T, Eisner L, Eckert GL, Danielson S (2009) Southeast Alaska: oceanographic habitats and linkages. J Biogeogr 36:387–400CrossRefGoogle Scholar
  68. Willson M F, Armstrong RH, Hermans MC, Koski K (2006) Eulachon: a review of biology and an annotated bibliography. Alaska Fish Sci Cent Processed Report 2006–12. Auke Bay Laboratory, Alaska Fish Sci Cent, NOAA, Natl Mar Fish ServGoogle Scholar
  69. Wilson MT, Jump CM, Buchheister A (2009) Ecology of small neritic fishes in the western Gulf of Alaska. II. Consumption of krill in relation to krill standing stock and the physical environment. Mar Ecol Prog Ser 392:239–251CrossRefGoogle Scholar
  70. Wischniowski SG, Kastelle CR, Loher T, Helser TE, Gillanders B (2015) Incorporation of bomb-produced 14 C into fish otoliths. An example of basin-specific rates from the North Pacific Ocean. Can J Fish Aquat Sci 72:879–892CrossRefGoogle Scholar
  71. Woodgate RA (2005) Revising the Bering Strait freshwater flux into the Arctic Ocean. Geophys Res Lett 32Google Scholar
  72. Yamamoto-Kawai M, Carmack EC, McLaughlin FA, Falkner KK (2010) Oxygen isotope ratio, barium and salinity in waters around the North American coast from the Pacific to the Atlantic: implications for freshwater sources to the Arctic throughflow. J Mar Res 68:97–117CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019

Authors and Affiliations

  1. 1.Resource Ecology and Fisheries ManagementAlaska Fisheries Science Center, National Marine Fisheries Service, NOAASeattleUSA

Personalised recommendations