Evaluation of the 137Ba mass-marking technique and potential effects in the early life history stages of Sepioteuthis lessoniana

Chun-I Chiang; Ming-Tsung Chung; Tung-Wei Shih; Tin-Yam Chan; Atsuko Yamaguchi; Chia-Hui Wang

doi:10.1071/MF18325

RESEARCH ARTICLE (Open Access)

Evaluation of the ¹³⁷Ba mass-marking technique and potential effects in the early life history stages of Sepioteuthis lessoniana

Chun-I Chiang ^A ^B , Ming-Tsung Chung ^C , Tung-Wei Shih ^D , Tin-Yam Chan ^A ^E , Atsuko Yamaguchi ^B and Chia-Hui Wang ^E ^F ^G

+ Author Affiliations

- Author Affiliations

^A Institute of Marine Biology, National Taiwan Ocean University, 2 Beining Road, Keelung, 20224, Taiwan.

^B Graduate School of Fisheries and Environmental Sciences, Nagasaki University, 1–14 Bunkyo, Nagasaki, 852-8521, Japan.

^C Department of Bioscience, Aquatic Biology, Aarhus University, Ole Worms Allé 1, DK-8000 Aarhus, Denmark.

^D National Museum of Marine Science and Technology, 367 Beining Road, Keelung, 20224, Taiwan.

^E Center of Excellence of the Oceans, National Taiwan Ocean University, 2 Beining Road, Keelung, 20224, Taiwan.

^F Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, 2 Beining Road, Keelung, 20224, Taiwan.

^G Corresponding author. Email: chwang99@ntou.edu.tw

Marine and Freshwater Research 70(12) 1698-1707 https://doi.org/10.1071/MF18325
Submitted: 3 September 2018 Accepted: 30 July 2019 Published: 22 October 2019

Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND

Abstract

The use of mass-marking techniques of enriched stable isotopes has increased in studies of ecology, movement patterns and the dispersal of marine organisms. However, the efficacy of this technique and its potential effects on hatchling size and statolith chemistry of cephalopods are yet to be investigated. Sepioteuthis lessoniana egg capsules were collected from northern Taiwan and assigned randomly to ¹³⁷Ba-spiking experimental groups at 0.2, 0.5 and 1 ppm and three immersion durations (1, 3 and 7 days). Immersion duration >3 days produced significantly lower ¹³⁸Ba : ¹³⁷Ba ratios, with 100% marking success, indicating that it is a reliable marking technique. The ¹³⁷Ba mass marking had a positive effect on size at hatch and was likely to affect statolith trace element incorporation, including Cu, Zn and Pb. These findings highlight that it is necessary to consider the species-specific effects on hatchling size and physiological responses in when using stable isotopes mass-marking techniques.

Additional keywords: barium isotopes, hatchling size, statolith chemistry.

References

Almany, G. R., Berumen, M. L., Thorrold, S. R., Planes, S., and Jones, G. P. (2007). Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744.
| Local replenishment of coral reef fish populations in a marine reserve.Crossref | GoogleScholarGoogle Scholar | 17478720PubMed |

Arkhipkin, A. I., Campana, S. E., FitzGerald, J., and Thorrold, S. R. (2004). Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi). Canadian Journal of Fisheries and Aquatic Sciences 61, 1212–1224.
| Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi).Crossref | GoogleScholarGoogle Scholar |

Barry, P. D., Tamone, S. L., and Tallmon, D. A. (2011). A comparison of tagging methodology for North Pacific giant octopus Enteroctopus dofleini. Fisheries Research 109, 370–372.
| A comparison of tagging methodology for North Pacific giant octopus Enteroctopus dofleini.Crossref | GoogleScholarGoogle Scholar |

Bernat, M., Church, T., and Allegre, C. J. (1972). Barium and strontium concentrations in Pacific and Mediterranean Sea water profiles by direct isotope dilution mass spectrometry. Earth and Planetary Science Letters 16, 75–80.
| Barium and strontium concentrations in Pacific and Mediterranean Sea water profiles by direct isotope dilution mass spectrometry.Crossref | GoogleScholarGoogle Scholar |

Blaxter, J. H. S. (1986). Development of sense organs and behavior of teleost larvae with special reference to feeding and predator avoidance. Transactions of the American Fisheries Society 115, 98–114.
| Development of sense organs and behavior of teleost larvae with special reference to feeding and predator avoidance.Crossref | GoogleScholarGoogle Scholar |

Bolger, T., and Connolly, P. L. (1989). The selection of suitable indices for the measurement and analysis of fish condition. Journal of Fish Biology 34, 171–182.
| The selection of suitable indices for the measurement and analysis of fish condition.Crossref | GoogleScholarGoogle Scholar |

Bower, S. M., and Margolis, L. (1991). Potential use of helminth parasites in stock identification of flying squid, Ommastrephes bartrami, in North Pacific Waters. Canadian Journal of Zoology 69, 1124–1126.
| Potential use of helminth parasites in stock identification of flying squid, Ommastrephes bartrami, in North Pacific Waters.Crossref | GoogleScholarGoogle Scholar |

Buresch, K. C., Gerlach, G., and Hanlon, R. T. (2006). Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter. Marine Ecology Progress Series 310, 263–270.
| Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter.Crossref | GoogleScholarGoogle Scholar |

Chen, D. S., Dykhuizen, G. V., Hodge, J., and Gilly, W. F. (1996). Ontogeny of copepod predation in juvenile squid (Loligo opalescens). The Biological Bulletin 190, 69–81.
| Ontogeny of copepod predation in juvenile squid (Loligo opalescens).Crossref | GoogleScholarGoogle Scholar | 8852631PubMed |

Clarke, M. R. (1996). Cephalopods in the world’s oceans: cephalopods as prey. III Cetaceans. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 351, 1053–1065.
| Cephalopods in the world’s oceans: cephalopods as prey. III Cetaceans.Crossref | GoogleScholarGoogle Scholar |

Cowen, R. K., and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.
| Larval dispersal and marine population connectivity.Crossref | GoogleScholarGoogle Scholar | 21141044PubMed |

Cowen, R. K., Lwiza, K. M. M., Sponaugle, S., Paris, C. B., and Olson, D. B. (2000). Connectivity of marine populations: open or closed? Science 287, 857–859.
| Connectivity of marine populations: open or closed?Crossref | GoogleScholarGoogle Scholar | 10657300PubMed |

Cronin, E. R., and Seymour, R. S. (2000). Respiration of the eggs of the giant cuttlefish Sepia apama. Marine Biology 136, 863–870.
| Respiration of the eggs of the giant cuttlefish Sepia apama.Crossref | GoogleScholarGoogle Scholar |

de Braux, E., Warren-Myers, F., Dempster, T., Fjelldal, P. G., Hansen, T., and Swearer, S. E. (2014). Osmotic induction improves batch marking of larval fish otoliths with enriched stable isotopes. ICES Journal of Marine Science 71, 2530–2538.
| Osmotic induction improves batch marking of larval fish otoliths with enriched stable isotopes.Crossref | GoogleScholarGoogle Scholar |

de Vries, M. C., Gillanders, B. M., and Elsdon, T. S. (2005). Facilitation of barium uptake into fish otoliths: influence of strontium concentration and salinity. Geochimica et Cosmochimica Acta 69, 4061–4072.
| Facilitation of barium uptake into fish otoliths: influence of strontium concentration and salinity.Crossref | GoogleScholarGoogle Scholar |

Fiorito, G., Affuso, A., Basil, J., Cole, A., de Girolamo, P., D’Angelo, L., Dickel, L., Gestal, C., Grasso, F., Kuba, M., Mark, F., Melillo, D., Osorio, D., Perkins, K., Ponte, G., Shashar, N., Smith, D., Smith, J., and Andrews, P. L. R. (2015). Guidelines for the care and welfare of cephalpods in research – a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Laboratory Animals 49, 1–90.
| Guidelines for the care and welfare of cephalpods in research – a consensus based on an initiative by CephRes, FELASA and the Boyd Group.Crossref | GoogleScholarGoogle Scholar | 26354955PubMed |

Forsythe, J. W. (2004). Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331–339.
| Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice.Crossref | GoogleScholarGoogle Scholar |

Gillanders, B. M., Wilkinson, L. M., Monro, A. R., and de Vries, M. C. (2013). Statolith chemistry of two life history stages of cuttlefish: effects of temperature and seawater trace element concentration. Geochimica et Cosmochimica Acta 101, 12–23.
| Statolith chemistry of two life history stages of cuttlefish: effects of temperature and seawater trace element concentration.Crossref | GoogleScholarGoogle Scholar |

Hall, K. C., and Fowler, A. J. (2003). The fisheries biology of the cuttlefish, Sepia apama Gray, in South Australian waters. FRDC final report, Project number 98/151, South Australian Research and Development Institute, Adelaide, SA, Australia.

Hamer, P. A., and Jenkins, G. P. (2007). Comparison of spatial variation in otolith chemistry of two fish species and relationships with water chemistry and otolith growth. Journal of Fish Biology 71, 1035–1055.
| Comparison of spatial variation in otolith chemistry of two fish species and relationships with water chemistry and otolith growth.Crossref | GoogleScholarGoogle Scholar |

Hunsicker, M. E., Essingtion, T. E., Watson, R., and Sumaila, U. R. (2010). The contribution of cephalopods to global marine fisheries: can we have our squid and eat them too? Fish and Fisheries 11, 421–438.
| The contribution of cephalopods to global marine fisheries: can we have our squid and eat them too?Crossref | GoogleScholarGoogle Scholar |

Ikeda, Y., Wada, Y., Arai, N., and Sakamoto, W. (1999). Note on size variation of body and statoliths in the oval squid Sepioteuthis lessoniana hatchlings. Journal of the Marine Biological Association of the United Kingdom 79, 757–759.
| Note on size variation of body and statoliths in the oval squid Sepioteuthis lessoniana hatchlings.Crossref | GoogleScholarGoogle Scholar |

Ikeda, Y., Yatsu, A., Arai, N., and 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. Journal of the Marine Biological Association of the United Kingdom 82, 863–866.
| Concentration of statolith trace elements in the jumbo flying squid during El Niño and non-El Niño years in the eastern Pacific.Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D., and Moltschaniwskyj, N. A. (2002). Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Marine Biology 140, 747–754.
| Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae).Crossref | GoogleScholarGoogle Scholar |

Jereb, P., and Roper, C. F. E. (2010). Sepioteuthis lessoniana Férussac in Lesson, 1831. In ‘Cephalopods of the World: an Annotated and Illustrated Catalogue of Cephalopod Species Known to Date, Volume 2. Myopisd and Oegopsid Squids’. (Eds P. Jereb and C. F. E. Roper.) FAO Species Catalogue for Fishery Purposes 4, pp. 95–97. (FAO: Rome, Italy.) Available at http://www.fao.org/3/i1920e/i1920e.pdf [Verified 5 September 2019].

Jones, G. P., Planes, S., and Thorrold, S. R. (2005). Coral reef fish larvae settle close to home. Current Biology 15, 1314–1318.
| Coral reef fish larvae settle close to home.Crossref | GoogleScholarGoogle Scholar | 16051176PubMed |

Kalish, J. M. (1989). Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition. Journal of Experimental Marine Biology and Ecology 132, 151–178.
| Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition.Crossref | GoogleScholarGoogle Scholar |

Klages, N. T. W. (1996). Cephalopods in the world’s oceans: cephalopods as prey. II Seals. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 351, 1045–1052.
| Cephalopods in the world’s oceans: cephalopods as prey. II Seals.Crossref | GoogleScholarGoogle Scholar |

Kresse, R., Baudis, U., Jäger, P., Riechers, H. H., Wagner, H., Winkler, J., and Wolf, H. U. (2007). Barium and barium compounds. In ‘Ullmann’s Encyclopedia of Industrial Chemistry’. (Ed. H. Pelc.) pp 621–640. (Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany.)10.1002/14356007.A03_325.PUB2

Lee, P. G., Turk, P. E., Yang, W. T., and Hanlon, R. T. (1994). Biological characteristics and biomedical applications of the squid Sepioteuthis lessoniana cultured through multiple generations. The Biological Bulletin 186, 328–341.
| Biological characteristics and biomedical applications of the squid Sepioteuthis lessoniana cultured through multiple generations.Crossref | GoogleScholarGoogle Scholar | 8043657PubMed |

Lloyd, D. C., Zacherl, D. C., Walker, S., Paradis, G., Sheehy, M., and Warner, R. R. (2008). Egg source, temperature and culture seawater affect elemental signatures in Kelletia kelletii larval statoliths. Marine Ecology Progress Series 353, 115–130.
| Egg source, temperature and culture seawater affect elemental signatures in Kelletia kelletii larval statoliths.Crossref | GoogleScholarGoogle Scholar |

Miller, B. M., Clough, A. M., Batson, J. N., and Vachet, R. W. (2006). Transition metal binding to cod otolith proteins. Journal of Experimental Marine Biology and Ecology 329, 135–143.
| Transition metal binding to cod otolith proteins.Crossref | GoogleScholarGoogle Scholar |

Munro, A. R., Gillanders, B. M., Elsdon, T. S., Crook, D. A., and Sanger, A. C. (2008). Enriched stable isotope marking of juvenile golded perch (Macquaria ambigua) otoliths. Canadian Journal of Fisheries and Aquatic Sciences 65, 276–285.
| Enriched stable isotope marking of juvenile golded perch (Macquaria ambigua) otoliths.Crossref | GoogleScholarGoogle Scholar |

Nagasawa, K., Takayanagi, S., and Takami, T. (1993). Cephalopod tagging and marking in Japan, a review. In ‘Recent Advances in Cephalopod Fisheries Biology’. (Eds T. Okutani, R. K. O’Dor, and T. Kuboera.) pp. 313–330. (Tokai University Press: Tokyo, Japan.)

Okutani, T. (2015). Sepioteuthis lessoniana Férussac in Lesson, 1832. In ‘Cuttlefishes and Squids of the World’. (Tokai University Press: Tokyo, Japan.) Available at http://www.zen-ika.com/zukan/pdf/cs184.pdf?idx=1 [Verified 6 September 2019].

Payne, N. L., Semmens, J. M., and Gillanders, B. M. (2011). Elemental uptake via immersion: a mass-marking technique for early life-history stages of cephalopods. Marine Ecology Progress Series 436, 169–176.
| Elemental uptake via immersion: a mass-marking technique for early life-history stages of cephalopods.Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T., Doubleday, Z. A., Danyushevsky, L., Gilbert, S., and Moltschaniwskyj, N. A. (2010). Transgenerational marking of cephalopods with an enriched barium isotope: a promising tool for empirically estimating post-hatching movement and population connectivity. ICES Journal of Marine Science 67, 1372–1380.
| Transgenerational marking of cephalopods with an enriched barium isotope: a promising tool for empirically estimating post-hatching movement and population connectivity.Crossref | GoogleScholarGoogle Scholar |

Replinger, S. E., and Wood, J. B. (2007). A preliminary investigation of the use of subcutaneous tagging in Caribbean reef squid Sepioteuthis sepioidea (Cephalopoda: Loliginidae). Fisheries Research 84, 308–313.
| A preliminary investigation of the use of subcutaneous tagging in Caribbean reef squid Sepioteuthis sepioidea (Cephalopoda: Loliginidae).Crossref | GoogleScholarGoogle Scholar |

Ricker, W. E. (1975). Computation and interpretation of biological statistics of fish population. Bulletin – Fisheries Research Board of Canada 191, 209–210.

Rosa, I. C., Raimundo, J., Lopes, V. M., Brandão, C., Couto, A., Santos, C., Cabecinhas, A. S., Cereja, R., Calado, R., Caetano, M., and Rosa, R. (2015). Cuttlefish capsule: an effective shield against contaminants in the wild. Chemosphere 135, 7–13.
| Cuttlefish capsule: an effective shield against contaminants in the wild.Crossref | GoogleScholarGoogle Scholar | 25876030PubMed |

Rosman, K. J. R., and Taylor, P. D. P. (1998). Isotopic compositions of the elements 1997 (technical report). Pure and Applied Chemistry 70, 217–235.
| Isotopic compositions of the elements 1997 (technical report).Crossref | GoogleScholarGoogle Scholar |

Sauer, W. H. H., Lipinski, M. R., and Augustyn, C. J. (2000). Tag recapture studies of the chokka squid Loligo vulgaris reynaudii d’Orbigny, 1845 on inshore spawning grounds on the south-east coast of South Africa. Fisheries Research 45, 283–289.
| Tag recapture studies of the chokka squid Loligo vulgaris reynaudii d’Orbigny, 1845 on inshore spawning grounds on the south-east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |

Segawa, S. (1987). Life history of the oval squid, Sepiothuthis lessoniana in Kominato and adjacent waters central Honshu, Japan. Journal of the Tokyo University of Fisheries 74, 67–105.

Semmens, J. M., Pecl, G. T., Gillanders, B. M., Waluda, C. M., Shea, E. K., Jouffre, D., Ichii, T., Zumholz, K., Katugin, O. N., Leporati, S. C., and Shaw, P. W. (2007). Approaches to resolving cephalopod movement and migration patterns. Reviews in Fish Biology and Fisheries 17, 401–423.
| Approaches to resolving cephalopod movement and migration patterns.Crossref | GoogleScholarGoogle Scholar |

Sinclair, D. J. (2005). Correlated trace element ‘vital effects’ in tropical corals: a new geochemical tool for probing biomineralization. Geochimica et Cosmochimica Acta 69, 3265–3284.
| Correlated trace element ‘vital effects’ in tropical corals: a new geochemical tool for probing biomineralization.Crossref | GoogleScholarGoogle Scholar |

Sinclair, D. J., and Risk, M. J. (2006). A numerical model of trace-element coprecipitation in a physicochemical calcification system: application to coral biomineralization and trace-element ‘vital effects’. Geochimica et Cosmochimica Acta 70, 3855–3868.
| A numerical model of trace-element coprecipitation in a physicochemical calcification system: application to coral biomineralization and trace-element ‘vital effects’.Crossref | GoogleScholarGoogle Scholar |

Smith, K. T., and Whitledge, G. W. (2011). Evaluation of a stable-isotope labelling technique for mass marking fin rays of age-0 lake sturgeon. Fisheries Management and Ecology 18, 168–175.
| Evaluation of a stable-isotope labelling technique for mass marking fin rays of age-0 lake sturgeon.Crossref | GoogleScholarGoogle Scholar |

Sogard, S. M. (1997). Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Science 60, 1129–1157.

Speer, J. A. (1983). Crystal chemistry and phase relations of orthorhombic carbonates. Reviews in Mineralogy and Geochemistry 11, 145–190.

Starrs, D., Ebner, B. C., Eggins, S. M., and Fulton, C. J. (2014a). Longevity in maternal transmission of isotopic marks. Marine and Freshwater Research 65, 400–408.
| Longevity in maternal transmission of isotopic marks.Crossref | GoogleScholarGoogle Scholar |

Starrs, D., Davis, J. T., Schlaefer, J., Ebner, B. C., Eggins, S. M., and Fulton, C. J. (2014b). Maternally transmitted isotopes and their effects on larval fish: a validation of dual isotopic marks with a meta-analysis. Canadian Journal of Fisheries and Aquatic Sciences 71, 387–397.
| Maternally transmitted isotopes and their effects on larval fish: a validation of dual isotopic marks with a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Sturrock, A. M., Hunter, E., Milton, J. A., EIMF Johnson, R. C., Waring, C. P., and Trueman, C. N. (2015). Quantifying physiological influences on otolith microchemistry. Methods in Ecology and Evolution 6, 806–816.
| Quantifying physiological influences on otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |

Sugimoto, C., and Ikeda, Y. (2013). Comparison of the ontogeny of hunting behavior in pharaoh cuttlefish (Sepia pharaonis) and oval squid (Sepioteuthis lessoniana). The Biological Bulletin 225, 50–59.
| Comparison of the ontogeny of hunting behavior in pharaoh cuttlefish (Sepia pharaonis) and oval squid (Sepioteuthis lessoniana).Crossref | GoogleScholarGoogle Scholar | 24088796PubMed |

Swearer, S. E., Caselle, J. E., Lea, D. W., and Warner, R. R. (1999). Larval retention and recruitment in an island population of a coral-reef fish. Nature 402, 799–802.
| Larval retention and recruitment in an island population of a coral-reef fish.Crossref | GoogleScholarGoogle Scholar |

Thorrold, S. R., Latkoczy, C., Swart, P. K., and Jones, C. M. (2001). Natal homing in a marine fish metapopulation. Science 291, 297–299.
| Natal homing in a marine fish metapopulation.Crossref | GoogleScholarGoogle Scholar | 11209078PubMed |

Thorrold, S. R., Jones, G. P., Planes, S., and Hare, J. A. (2006). Transgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes. Canadian Journal of Fisheries and Aquatic Sciences 63, 1193–1197.
| Transgenerational marking of embryonic otoliths in marine fishes using barium stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Walther, B. D., Kingsford, M. J., O’Callaghan, M. D., and McCullonch, M. T. (2010). Interaction effects of ontogeny, food ration and temperature on elemental incorporation in otoliths of a coral reef fish. Environmental Biology of Fishes 89, 441–451.
| Interaction effects of ontogeny, food ration and temperature on elemental incorporation in otoliths of a coral reef fish.Crossref | GoogleScholarGoogle Scholar |

Warren-Myers, F., Dempster, T., Fjelldal, P. G., Hansen, T., and Swearer, S. E. (2015). Immersion during egg swelling results in rapid uptake of stable isotope markers in salmonid otoliths. Canadian Journal of Fisheries and Aquatic Sciences 72, 722–727.
| Immersion during egg swelling results in rapid uptake of stable isotope markers in salmonid otoliths.Crossref | GoogleScholarGoogle Scholar |

Warren-Myers, F., Dempster, T., and Swearer, S. E. (2018). Otolith mass marking techniques for aquaculture and restocking: benefits and limitations. Reviews in Fish Biology and Fisheries 28, 485–501.
| Otolith mass marking techniques for aquaculture and restocking: benefits and limitations.Crossref | GoogleScholarGoogle Scholar |

Williamson, D. H., Jones, G. P., and Thorrold, S. R. (2009). An experimental evaluation of transgenerational isotope labelling in a coral reef grouper. Marine Biology 156, 2517–2525.
| An experimental evaluation of transgenerational isotope labelling in a coral reef grouper.Crossref | GoogleScholarGoogle Scholar |

Woodcock, S. H., and Walther, B. D. (2014). Concentration-dependent mixing models predict values of diet-derived stable isotope ratios in fish otoliths. Journal of Experimental Marine Biology and Ecology 454, 63–69.
| Concentration-dependent mixing models predict values of diet-derived stable isotope ratios in fish otoliths.Crossref | GoogleScholarGoogle Scholar |

Woodcock, S. H., Gillanders, B. M., Munro, A. R., McGovern, F., Crook, D. A., and Sanger, A. C. (2011a). Using enriched stable isotopes of barium and magnesium to batch mark otoliths of larval golden perch (Macquaria ambigua, Richardson). Ecology Freshwater Fish 20, 157–165.
| Using enriched stable isotopes of barium and magnesium to batch mark otoliths of larval golden perch (Macquaria ambigua, Richardson).Crossref | GoogleScholarGoogle Scholar |

Woodcock, S. H., Gillanders, B. M., Munro, A. R., Crook, D. A., and Sanger, A. C. (2011b). Determining mark success of 15 combinations of enriched stable isotopes for the batch marking of larval otoliths. North American Journal of Fisheries Management 31, 843–851.
| Determining mark success of 15 combinations of enriched stable isotopes for the batch marking of larval otoliths.Crossref | GoogleScholarGoogle Scholar |

Zitek, A., Irrgeher, J., Kletzl, M., Weismann, T., and Prohaska, T. (2013). Transgenerational marking of brown trout Salmo trutta f.f. using an 84Sr spike. Fisheries Management and Ecology 20, 354–361.
| Transgenerational marking of brown trout Salmo trutta f.f. using an ⁸⁴Sr spike.Crossref | GoogleScholarGoogle Scholar |

Zumholz, K., Hansteen, T. H., Piatkowski, U., and Crrot, P. L. (2007). Influence of temperature and salinity on the trace element incorporation into statoliths of the common cuttlefish (Sepia officinalis). Marine Biology 151, 1321–1330.
| Influence of temperature and salinity on the trace element incorporation into statoliths of the common cuttlefish (Sepia officinalis).Crossref | GoogleScholarGoogle Scholar |