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Estimating migration patterns of fish from otolith chemical composition time series

Publication: Canadian Journal of Fisheries and Aquatic Sciences
10 April 2021

Abstract

Understanding migration patterns and habitat use is of great importance for management and conservation of marine living resources. The chemical composition of otoliths is influenced by the surrounding environment; therefore, they are indispensable data archives. To extract migration patterns and historical habitat use of individual fish, we analyse otolith chemical compositions obtained by laser ablation inductively coupled plasma mass spectrometry by a regime-switching state-space model. The state-space model filters the measurement noise from the environmental signal. In turn, the filtered signal is converted to geographical positions through a calibration of strontium to salinity. The method is validated by a simulation study and applied to 404 Atlantic cod (Gadus morhua) otoliths.

Résumé

La compréhension des habitudes migratoires et de l’utilisation de l’habitat est d’une grande importance pour la gestion et la conservation des ressources marines vivantes. Parce que leur composition chimique est influencée par le milieu environnant, les otolites constituent d’indispensables archives de données. Afin d’inférer les habitudes migratoires et d’utilisation de l’habitat passées de poissons individuels, nous analysons la composition chimique d’otolites obtenue par spectrométrie de masse avec plasma à couplage inductif jumelée à l’ablation au laser (LA-ICP-MS) à l’aide d’un modèle d’espace d’états des changements de régime. Ce modèle filtre le bruit de mesure du signal du milieu ambiant. Le signal filtré est ensuite converti en positions géographiques par l’étalonnage du strontium en fonction de la salinité. La méthode est validée par une étude de simulation et appliquée à 404 otolites de morue (Gadus morhua). [Traduit par la Rédaction]

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References

Albertsen, C.M. 2018. State-space modelling in marine science, Ph.D. thesis, Technical University of Denmark, National Institute of Aquatic Resources.
Albuquerque C.Q., Miekeley N., Muelbert J.H., Walther B.D., and Jaureguizar A.J. 2012. Estuarine dependency in a marine fish evaluated with otolith chemistry. Mar. Biol. 159(10): 2229–2239.
Altenritter M., Cohuo A., and Walther B. 2018. Proportions of demersal fish exposed to sublethal hypoxia revealed by otolith chemistry. Mar. Ecol. Prog. Ser. 589: 193–208.
Barnes T.C. and Gillanders B.M. 2013. Combined effects of extrinsic and intrinsic factors on otolith chemistry: implications for environmental reconstructions. Can. J. Fish. Aquat. Sci. 70(8): 1159–1166.
Bath G.E., Thorrold S.R., Jones C.M., Campana S.E., McLaren J.W., and Lam J.W. 2000. Strontium and barium uptake in aragonitic otoliths of marine fish. Geochim. Cosmochim. Acta, 64(10): 1705–1714.
Bauer R., Stepputtis D., Storr-Paulsen M., Weigelt R., and Hammer C. 2010. Estimating abundances of 0-group western baltic cod by using pound net fisheries. Informationen aus der Fischereiforschung, 57(1): 1–11.
Begg G.A., Campana S.E., Fowler A.J., and Suthers I.M. 2005. Otolith research and application: current directions in innovation and implementation. Mar. Freshwater Res. 56(5): 477–483.
Bivand, R.S., Pebesma, E., and Gomez-Rubio, V. 2013. Applied spatial data analysis with R. 2nd ed. Springer, New York.
Campana S.E., Chouinard G.A., Hanson J.M., and Fréchet A. 1999. Mixing and migration of overwintering atlantic cod (gadus morhua) stocks near the mouth of the gulf of st. lawrence. Can. J. Fish. Aquat. Sci. 56(10): 1873–1881.
Cappo M., De'ath G., Boyle S., Aumend J., Olbrich R., Hoedt F., et al. 2005. Development of a robust classifier of freshwater residence in barramundi (lates calcarifer) life histories using elemental ratios in scales and boosted regression trees. Mar. Freshwater Res. 56(5): 713–723.
DiMaria R.A., Miller J.A., and Hurst T.P. 2010. Temperature and growth effects on otolith elemental chemistry of larval pacific cod, gadus macrocephalus. Environ. Biol. Fish. 89(3–4): 453–462.
Edmonds J.S., Moran M.J., Caputi N., and Morita M. 1989. Trace element analysis of fish sagittae as an aid to stock identifications: Pink snapper (Chrysophrys auratus) in western Australian waters. Can. J. Fish. Aquat. Sci. 46(1): 50–54.
Elsdon T.S. and Gillanders B.M. 2002. Interactive effects of temperature and salinity on otolith chemistry: challenges for determining environmental histories of fish. Can. J. Fish. Aquat. Sci. 59(11): 1796–1808.
Elsdon T.S. and Gillanders B.M. 2003. Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri. Mar. Ecol. Prog. Ser. 260: 263–272.
Elsdon T.S. and Gillanders B.M. 2004. Fish otolith chemistry influenced by exposure to multiple environmental variables. J. Exp. Mar. Biol. Ecol. 313(2): 269–284.
Elsdon T.S. and Gillanders B.M. 2005a. Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency. Can. J. Fish. Aquat. Sci. 62(5): 1143–1152.
Elsdon T.S. and Gillanders B.M. 2005b. Consistency of patterns between laboratory experiments and field collected fish in otolith chemistry: an example and applications for salinity reconstructions. Mar. Freshwater Res. 56(5): 609–617.
Fablet R., Daverat F., and De Pontual H. 2007. Unsupervised Bayesian reconstruction of individual life histories from otolith signatures: case study of Sr:Ca transects of European eel (Anguilla anguilla) otoliths. Can. J. Fish. Aquat. Sci. 64(1): 152–165.
Fowler A.J., Campana S.E., Thorrold S.R., and Jones C.M. 1995. Experimental assessment of the effect of temperature and salinity on elemental composition of otoliths using solution-based ICPMS. Can. J. Fish. Aquat. Sci. 52(7): 1421–1430.
Gallagher B.K., Piccoli P.M., and Secor D.H. 2018. Ecological carryover effects associated with partial migration in white perch (Morone americana) within the Hudson River Estuary. Estuarine Coastal Shelf Sci. 200: 277–288.
Gallaghar N. and Kingsford M.J. 1996. Factors influencing Sr/Ca ratios in otoliths of Girella elevata: an experimental investigation. J. Fish Biol. 48(2): 174–186.
Gibb F.M., Régnier T., Donald K., and Wright P.J. 2017. Connectivity in the early life history of sandeel inferred from otolith microchemistry. J. Sea Res. 119: 8–16.
Global Monitoring and Forecasting Center. 2019a. Baltic Sea biogeochemistry reanalysis product. E.U. Copernicus Marine Service Information [Data set]. Available from https://resources.marine.copernicus.eu/product-detail/BALTICSEA_REANALYSIS_BIO_003_012/INFORMATION [accessed 19 March 2019].
Global Monitoring and Forecasting Center. 2019b. Global ocean 1/12° physics analysis and forecast updated daily product. E.U. Copernicus Marine Service Information [Data set]. Available from https://resources.marine.copernicus.eu/product-detail/GLOBAL_ANALYSIS_FORECAST_PHY_001_024/INFORMATION [accessed 19 March 2019].
Grammer G.L., Morrongiello J.R., Izzo C., Hawthorne P.J., Middleton J.F., and Gillanders B.M. 2017. Coupling biogeochemical tracers with fish growth reveals physiological and environmental controls on otolith chemistry. Ecol. Monogr. 87(3): 487–507.
Hamer P.A., Jenkins G.P., and Coutin P. 2006. Barium variation in Pagrus auratus (Sparidae) otoliths: a potential indicator of migration between an embayment and ocean waters in south-eastern Australia. Estuarine Coastal Shelf Sci. 68(3–4): 686–702.
Hedger R.D., Atkinson P.M., Thibault I., and Dodson J.J. 2008. A quantitative approach for classifying fish otolith strontium: calcium sequences into environmental histories. Ecol. Inf. 3(3): 207–217.
Heidemann F., Marohn L., Hinrichsen H., Huwer B., Hüssy K., Klügel A., et al. 2012. Suitability of otolith microchemistry for stock separation of baltic cod. Mar. Ecol. Prog. Ser. 465: 217–226.
Hemmer-Hansen J., Hüssy K., Baktoft H., Huwer B., Bekkevold D., Haslob H., et al. 2019. Genetic analyses reveal complex dynamics within a marine fish management area. Evol. Appl. 12(4): 830–844.
Hemmer-Hansen, J., Hüssy, K., Vinther, M., Albertsen, C., Storr-Paulsen, M., and Eero, M. 2020. Sustainable management of Kattegat cod; better knowledge of stock components and migration. DTU Aqua Report 357-2020. National Institute of Aquatic Resources, Technical University of Denmark.
Hicks A.S., Closs G.P., and Swearer S.E. 2010. Otolith microchemistry of two amphidromous galaxiids across an experimental salinity gradient: a multi-element approach for tracking diadromous migrations. J. Exp. Mar. Biol. Ecol. 394(1–2): 86–97.
Hijmans, R.J. 2018. raster: geographic data analysis and modeling. R package version 2.8-4.
Hughes J.M., Stewart J., Gillanders B.M., Collins D., and Suthers I.M. 2016. Relationship between otolith chemistry and age in a widespread pelagic teleost arripis trutta: influence of adult movements on stock structure and implications for management. Mar. Freshwater Res. 67(2): 224–237.
Hüssy K., Andersen N.G., and Pedersen E.M. 2016. The influence of feeding behaviour on growth of Atlantic cod (Gadus morhua, Linnaeus, 1758) in the North Sea. J. Appl. Ichthyol. 32(5): 928–937.
Hüssy K., Limburg K.E., de Pontual H., Thomas O.R.B., Cook P.K., Heimbrand Y., et al. 2020. Trace element patterns in otoliths: the role of biomineralization. Rev. Fish. Sci. Aquacult. 1–33.
Jessop B., Shiao J., Iizuka Y., and Tzeng W. 2002. Migratory behaviour and habitat use by American eels Anguilla rostrata as revealed by otolith microchemistry. Mar. Ecol. Prog. Ser. 233: 217–229.
Jessop B., Cairns D., Thibault I., and Tzeng W. 2008. Life history of American eel Anguilla rostrata: new insights from otolith microchemistry. Aquat. Biol. 1: 205–216.
Kalish J.M. 1989. Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition. J. Exp. Mar. Biol. Ecol. 132(3): 151–178.
Kennedy B.P., Klaue A., Blum J.D., Folt C.L., and Nislow K.H. 2002. Reconstructing the lives of fish using Sr isotopes in otoliths. Can. J. Fish. Aquat. Sci. 59(6): 925–929.
Kraus R.T. and Secor D.H. 2004. Incorporation of strontium into otoliths of an estuarine fish. J. Exp. Mar. Biol. Ecol. 302(1): 85–106.
Kristensen K., Nielsen A., Berg C.W., Skaug H., and Bell B.M. 2016. TMB: automatic differentiation and Laplace approximation. J. Stat. Soft. 70(5): 1–21.
Limburg K. 1995. Otolith strontium traces environmental history of subyearling American shad Alosa sapidissima. Mar. Ecol. Prog. Ser. 119: 25–35.
Limburg K.E., Olson C., Walther Y., Dale D., Slomp C.P., and Hoie H. 2011. Tracking Baltic hypoxia and cod migration over millennia with natural tags. Proc. Natl. Acad. Sci. U.S.A. 108(22): E177–E182.
Limburg K.E., Walther B.D., Lu Z., Jackman G., Mohan J., Walther Y., et al. 2015. In search of the dead zone: use of otoliths for tracking fish exposure to hypoxia. J. Mar. Syst. 141: 167–178.
Lin S.-H., Chang C.-W., Iizuka Y., and Tzeng W.-N. 2007. Salinities, not diets, affect strontium/calcium ratios in otoliths of Anguilla japonica. J. Exp. Mar. Biol. Ecol. 341(2): 254–263.
Loewen T.N., Reist J.D., Yang P., Koleszar A., Babaluk J.A., Mochnacz N., and Halden N.M. 2015. Discrimination of northern form Dolly Varden Char (Salvelinus malma malma) stocks of the North Slope, Yukon and Northwest Territories, Canada via otolith trace elements and 87Sr/86Sr isotopes. Fish. Res. 170: 116–124.
Martin G. and Wuenschel M. 2006. Effect of temperature and salinity on otolith element incorporation in juvenile gray snapper Lutjanus griseus. Mar. Ecol. Prog. Ser. 324: 229–239.
Mercier L., Mouillot D., Bruguier O., Vigliola L., and Darnaude A. 2012. Multi-element otolith fingerprints unravel sea-lagoon lifetime migrations of gilthead sea bream Sparus aurata. Mar. Ecol. Prog. Ser. 444: 175–194.
Miller J. 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(1–2): 42–52.
Morissette O., Lecomte F., Verreault G., Legault M., and Sirois P. 2016. Fully equipped to succeed: Migratory contingents seen as an intrinsic potential for striped bass to exploit a heterogeneous environment early in life. Estuaries Coasts, 39(2): 571–582.
Nielsen E.E., Cariani A., Aoidh E.M., Maes G.E., Milano I., Ogden R., et al. 2012. Gene-associated markers provide tools for tackling illegal fishing and false eco-certification. Nat. Commun. 3: 851.
Oeberst, R. 2008. Distribution pattern of cod and flounder in the Baltic sea based on international coordinated trawl surveys. ICES CM 2008/J:09.
Pebesma E.J. and Bivand R.S. 2005. Classes and methods for spatial data: the sp package. R News, 5(2): 9–13.
Pihl L. 1993. Migration pattern of juvenile cod (Gadus morhua) on the Swedish west coast. ICES J. Mar. Sci. 50(1): 63–70.
R Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Ranaldi M.M. and Gagnon M.M. 2008. Trace metal incorporation in otoliths of black bream (Acanthopagrus butcheri Munro), an indicator of exposure to metal contamination. Water Air Soil Pollut. 194(1–4): 31–43.
Reis-Santos P., Tanner S.E., Elsdon T.S., Cabral H.N., and Gillanders B.M. 2013. Effects of temperature, salinity and water composition on otolith elemental incorporation of Dicentrarchus labrax. J. Exp. Mar. Biol. Ecol. 446: 245–252.
Roberts B.H., Morrongiello J.R., King A.J., Morgan D.L., Saunders T.M., Woodhead J., and Crook D.A. 2019. Migration to freshwater increases growth rates in a facultatively catadromous tropical fish. Oecologia, 191(2): 253–260.
Sadovy Y. and Severin K. 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). Bull. Mar. Sci. 50(2): 237–257.
Sakamoto T., Komatsu K., Shirai K., Higuchi T., Ishimura T., Setou T., et al. 2019. Combining microvolume isotope analysis and numerical simulation to reproduce fish migration history. Methods Ecol. Evol. 10(1): 59–69.
Secor D.H. and Piccoli P.M. 1996. Age- and sex-dependent migrations of striped bass in the Hudson River as determined by chemical microanalysis of otoliths. Estuaries, 19(4): 778–793.
Secor D.H. and Rooker J.R. 2000. Is otolith strontium a useful scalar of life cycles in estuarine fishes? Fish. Res. 46(1–3): 359–371.
Secor D.H., Henderson-Arzapalo A., and Piccoli P. 1995. Can otolith microchemistry chart patterns of migration and habitat utilization in anadromous fishes? J. Exp. Mar. Biol. Ecol. 192(1): 15–33.
Seeley M. and Walther B. 2018. Facultative oligohaline habitat use in a mobile fish inferred from scale chemistry. Mar. Ecol. Prog. Ser. 598: 233–245.
Seeley M.E., Logan W.K., and Walther B.D. 2017. Consistency of elemental and isotope-ratio patterns across multiple scales from individual fish. J. Fish Biol. 91(3): 928–946.
Serre S., Nielsen K., Fink-Jensen P., Thomsen T., and Hüssy K. 2018. Analysis of cod otolith microchemistry by continuous line transects using LA-ICP-MS. Geol. Surv. Den. Greenl. Bull. 41: 91–94.
South, A. 2012. rworldxtra: country boundaries at high resolution. R package version 1.01.
Stanley R.R.E., Bradbury I.R., DiBacco C., Snelgrove P.V.R., Thorrold S.R., and Killen S.S. 2015. Environmentally mediated trends in otolith composition of juvenile Atlantic cod (Gadus morhua). ICES J. Mar. Sci. 72(8): 2350–2363.
Sturrock A.M., Trueman C.N., Darnaude A.M., and Hunter E. 2012. Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? J. Fish Biol. 81(2): 766–795.
Sturrock A.M., Hunter E., Milton J.A., Johnson R.C., Waring C.P., and Tureman C.N. 2015. Quantifying physiological influences on otolith microchemistry. Methods Ecol. Evol. 6(7): 806–816.
Tzeng W.-N. 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(1): 111–122.
Vitale, F., Worsøe Clausen, L., and Ní Chonchúir, G. 2019. Handbook of fish age estimation protocols and validation methods. ICES Cooperative Research Report 346. International Council for the Exploration of the Sea, Copenhagen, Denmark.
Walther B.D. and Limburg K.E. 2012. The use of otolith chemistry to characterize diadromous migrations. J. Fish Biol. 81(2): 796–825.
Walther B.D., Kingsford M.J., O’Callaghan M.D., and McCulloch M.T. 2010. Interactive effects of ontogeny, food ration and temperature on elemental incorporation in otoliths of a coral reef fish. Environ. Biol. Fish. 89(3–4): 441–451.
Zimmerman C.E. 2005. Relationship of otolith strontium-to-calcium ratios and salinity: experimental validation for juvenile salmonids. Can. J. Fish. Aquat. Sci. 62(1): 88–97.

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cover image Canadian Journal of Fisheries and Aquatic Sciences
Canadian Journal of Fisheries and Aquatic Sciences
Volume 78Number 10October 2021
Pages: 1512 - 1523

History

Received: 23 September 2020
Accepted: 5 April 2021
Accepted manuscript online: 10 April 2021
Version of record online: 10 April 2021

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Christoffer Moesgaard Albertsen [email protected]
National Institute of Aquatic Resources, Technical University of Denmark, Kemitorvet 201, Kgs. Lyngby DK-2800, Denmark.
Karin Hüssy
National Institute of Aquatic Resources, Technical University of Denmark, Kemitorvet 201, Kgs. Lyngby DK-2800, Denmark.
Simon Hansen Serre
Geological Survey of Denmark and Greenland, Øster Voldgade 10, Copenhagen DK-1350, Denmark.
Jakob Hemmer-Hansen
National Institute of Aquatic Resources, Technical University of Denmark, Vejlsøvej 39, Silkeborg DK-8600, Denmark.
Tonny Bernt Thomsen
Geological Survey of Denmark and Greenland, Øster Voldgade 10, Copenhagen DK-1350, Denmark.

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© 2021 The Author(s). Permission for reuse (free in most cases) can be obtained from copyright.com.

Funding Information

Danish Ministry for Environment and Food and the European Union: 33113-B-16-034
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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