Element composition of shark vertebrae shows promise as a natural tag
J. C. A. Pistevos
A B E , P. Reis-Santos A C , C. Izzo A D and B. M. Gillanders A
+ Author Affiliations
- Author Affiliations
A Southern Seas Ecology Laboratories, School of Biological Sciences, The University of Adelaide, SA 5005, Australia.
B Paris Sciences et Lettres (PSL) Research University, EPHE-UPVD-CNRS, USR 3278 CRIOBE and Laboratoire d’Excellence CORAIL, BP 1013, 98729 Papetoai, Moorea, French Polynesia.
C MARE – Marine and Environmental Sciences Centre, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, PT-1749-016, Lisboa, Portugal.
D Fisheries Research and Development Corporation, PO Box 2733, Kent Town, SA 5071, Australia.
E Corresponding author. Email: jennifer.pistevos@ephe.sorbonne.fr
Marine and Freshwater Research 70(12) 1722-1733 https://doi.org/10.1071/MF18423
Submitted: 2 November 2018 Accepted: 1 May 2019 Published: 13 August 2019
Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND
Abstract
Reconstructing movements and environmental histories of sharks may be possible by using the element composition of vertebrae, but unlocking such possibilities requires an understanding of the effects of extrinsic and intrinsic factors on element composition. We assessed water temperature and pH effects (independently and in combination) on vertebral chemistry of Port Jackson sharks while accounting for intrinsic factors (condition and sex) using indoor aquaria and outdoor mesocosm environments, where the latter may better reflect natural field conditions. We analysed eight element : Ca ratios (7Li, 8B, 24Mg, 55Mn, 65Cu, 88Sr, 138Ba and 238U) by laser ablation inductively coupled plasma mass spectrometry and found positive temperature-dependant responses for multiple elements, including B : Ca, Mn : Ca, Sr : Ca and Ba : Ca (r2 = 0.43, 0.22, 0.60 and 0.35 respectively), whereas pH had a minor effect on vertebral Mg : Ca and Li : Ca (r2 = 0.10 and 0.31 respectively). As shown for teleost otoliths, condition affected element composition (Mn : Ca), suggesting potential physiological influences on element uptake. The suitability of vertebral chemistry as a natural tag appears to be element specific, and likely governed by a suite of potentially codependent extrinsic and intrinsic factors. Overall, variations in vertebrae chemistry show promise to reconstruct movements and habitat use of cartilaginous fishes. Yet, further research is required to understand the ubiquitous nature of the findings presented here.
Additional keywords: acidification, condition, elasmobranchs, Heterodontus portusjacksoni, hydroxyapatite, vertebrae chemistry.
References
Bartoń, K. (2019). Package ‘MuMIn’, ver. 1.43.6. Available at https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf [Verified 8 August 2019].Bath, G. H., Thorrold, S. T., Jones, C. M., Campana, S. E., McLaren, J. W., and Lam, J. W. (2000). Strontium and barium uptake in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 64, 1705–1714.
| Strontium and barium uptake in aragonitic otoliths of marine fish.Crossref | GoogleScholarGoogle Scholar |
Cailliet, G. M., Goldman, K. J., Carrier, J. C., Musick, J. A., and Heithaus, M. R. (2004). Age determination and validation in chondrichthyans fishes. In ‘Biology of Sharks and Their Relatives’. (Eds J. Carrier, J. A. Musick, and M. Heithaus.) pp. 399–447. (CRC Press: San Diego, CA, USA.)
Cailliet, G. M., Smith, W. D., Mollet, H. F., and Goldman, K. J. (2006). Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting. Environmental Biology of Fishes 77, 211–228.
| Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting.Crossref | GoogleScholarGoogle Scholar |
Campana, S. E. (1999). Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.
| Chemistry and composition of fish otoliths: pathways, mechanisms and applications.Crossref | GoogleScholarGoogle Scholar |
Cattano, C., Claudet, J., Domenici, P., and Milazzo, M. (2018). Living in a high CO2 world: a global meta‐analysis shows multiple trait‐mediated fish responses to ocean acidification. Ecological Monographs 88, 320–335.
| Living in a high CO2 world: a global meta‐analysis shows multiple trait‐mediated fish responses to ocean acidification.Crossref | GoogleScholarGoogle Scholar |
Chang, M., and Geffen, A. J. (2013). Taxonomic and geographic influences on fish otolith microchemistry. Fish and Fisheries 14, 458–492.
| Taxonomic and geographic influences on fish otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Clarke, L. M., Thorrold, S. R., and Conover, D. O. (2011). Population differences in otolith chemistry have a genetic basis in Menidia menidia. Canadian Journal of Fisheries and Aquatic Sciences 68, 105–114.
| Population differences in otolith chemistry have a genetic basis in Menidia menidia.Crossref | GoogleScholarGoogle Scholar |
Clement, J. (1992). Re-examination of the fine structure of endoskeletal mineralization in Chondrichthyans: implications for growth, ageing and calcium homeostasis. Marine and Freshwater Research 43, 157–181.
| Re-examination of the fine structure of endoskeletal mineralization in Chondrichthyans: implications for growth, ageing and calcium homeostasis.Crossref | GoogleScholarGoogle Scholar |
Dean, M. N., and Summers, A. P. (2006). Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology 109, 164–168.
| Mineralized cartilage in the skeleton of chondrichthyan fishes.Crossref | GoogleScholarGoogle Scholar | 16584875PubMed |
Dean, M. N., Ekstrom, L., Monsonego-Ornan, E., Ballantyne, J., Witten, E. P., Riley, C., Habraken, W., and Omelon, S. (2015). Mineral homeostasis and regulation of mineralization processes in the skeletons of sharks, rays and relatives (Elasmobranchii). Seminars in Cell & Developmental Biology 46, 51–67.
| Mineral homeostasis and regulation of mineralization processes in the skeletons of sharks, rays and relatives (Elasmobranchii).Crossref | GoogleScholarGoogle Scholar |
DiMaria, R., Miller, J., and Hurst, T. (2010). Temperature and growth effects on otolith elemental chemistry of larval Pacific cod, Gadus macrocephalus. Environmental Biology of Fishes 89, 453–462.
| Temperature and growth effects on otolith elemental chemistry of larval Pacific cod, Gadus macrocephalus.Crossref | GoogleScholarGoogle Scholar |
Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Marketing Science 1, 169–192.
| Ocean acidification: the other CO2 problem.Crossref | GoogleScholarGoogle Scholar |
Doubleday, Z., Izzo, C., Woodcock, S., and Gillanders, B. (2013). Relative contribution of water and diet to otolith chemistry in freshwater fish. Aquatic Biology 18, 271–280.
| Relative contribution of water and diet to otolith chemistry in freshwater fish.Crossref | GoogleScholarGoogle Scholar |
Doubleday, Z. A., Nagelkerken, I., and Connell, S. D. (2017). Ocean life breaking rules by building shells in acidic extremes. Current Biology 27, R1104–R1106.
| Ocean life breaking rules by building shells in acidic extremes.Crossref | GoogleScholarGoogle Scholar | 29065288PubMed |
Elsdon, T., and Gillanders, B. (2003). Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri. Marine Ecology Progress Series 260, 263–272.
| Relationship between water and otolith elemental concentrations in juvenile black bream Acanthopagrus butcheri.Crossref | GoogleScholarGoogle Scholar |
Elsdon, T., and Gillanders, B. (2005). Consistency of patterns between laboratory experiments and field collected fish in otolith chemistry: an example and applications for salinity reconstructions. Marine and Freshwater Research 56, 609–617.
| Consistency of patterns between laboratory experiments and field collected fish in otolith chemistry: an example and applications for salinity reconstructions.Crossref | GoogleScholarGoogle Scholar |
Elsdon, T. S., Wells, B. K., Campana, S. E., Gillanders, B. M., Jones, C. M., Limburg, K. E., Secor, D. H., Thorrold, S. R., and Walther, B. D. (2008). Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences. Oceanography and Marine Biology – an Annual Review 46, 297–330.
| Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations and inferences.Crossref | GoogleScholarGoogle Scholar |
Fablet, R., Pecquerie, L., de Pontual, H., Høie, H., Millner, R., Mosegaard, H., and Kooijman, S. A. (2011). Shedding light on fish otolith biomineralization using a bioenergetic approach. PLoS One 6, e27055.
| Shedding light on fish otolith biomineralization using a bioenergetic approach.Crossref | GoogleScholarGoogle Scholar | 22110601PubMed |
Fleishman, D. G., Saulus, A. A., and Vasilieva, V. F. (1986). Lithium in marine elasmobranchs as a natural marker of rectal gland contribution in sodium balance. Comparative Biochemistry and Physiology – A. Physiology 84, 643–648.
| Lithium in marine elasmobranchs as a natural marker of rectal gland contribution in sodium balance.Crossref | GoogleScholarGoogle Scholar |
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 laser ablation ICPMS. Canadian Journal of Fisheries and Aquatic Sciences 52, 1431–1441.
| Experimental assessment of the effect of temperature and salinity on elemental composition of otoliths using laser ablation ICPMS.Crossref | GoogleScholarGoogle Scholar |
Frieder, C. A., Gonzalez, J. P., and Levin, L. A. (2014). Uranium in larval shells as a barometer of molluscan ocean acidification exposure. Environmental Science & Technology 48, 6401–6408.
| Uranium in larval shells as a barometer of molluscan ocean acidification exposure.Crossref | GoogleScholarGoogle Scholar |
Gillanders, B. M., Elsdon, T. S., Halliday, I. A., Jenkins, G. P., Robins, J. B., and Valesini, F. J. (2011). Potential effects of climate change on Australian estuaries and fish utilising estuaries: a review. Marine and Freshwater Research 62, 1115–1131.
| Potential effects of climate change on Australian estuaries and fish utilising estuaries: a review.Crossref | GoogleScholarGoogle Scholar |
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. Ecological Monographs 87, 487–507.
| Coupling biogeochemical tracers with fish growth reveals physiological and environmental controls on otolith chemistry.Crossref | GoogleScholarGoogle Scholar |
Green, L., and Jutfelt, F. (2014). Elevated carbon dioxide alters the plasma composition and behaviour of a shark. Biology Letters 10, 20140538.
| Elevated carbon dioxide alters the plasma composition and behaviour of a shark.Crossref | GoogleScholarGoogle Scholar | 25232027PubMed |
Grønkjær, P. (2016). Otoliths as individual indicators: a reappraisal of the link between fish physiology and otolith characteristics. Marine and Freshwater Research 67, 881–888.
| Otoliths as individual indicators: a reappraisal of the link between fish physiology and otolith characteristics.Crossref | GoogleScholarGoogle Scholar |
Handley-Sidhu, S., Mullan, T. K., Grail, Q., Albadarneh, M., Ohnuki, T., and Macaskie, L. E. (2016). Influence of pH, competing ions, and salinity on the sorption of strontium and cobalt onto biogenic hydroxyapatite. Scientific Reports 6, 23361.
| Influence of pH, competing ions, and salinity on the sorption of strontium and cobalt onto biogenic hydroxyapatite.Crossref | GoogleScholarGoogle Scholar | 26988070PubMed |
Harvey, B. P., Gwynn‐Jones, D., and Moore, P. J. (2013). Meta‐analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution 3, 1016–1030.
| Meta‐analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming.Crossref | GoogleScholarGoogle Scholar | 23610641PubMed |
Hinojosa, J. L., Brown, S. T., Chen, J., DePaolo, D. J., Paytan, A., Shen, S., and Payne, J. L. (2012). Evidence for end-Permian ocean acidification from calcium isotopes in biogenic apatite. Geology 40, 743–746.
| Evidence for end-Permian ocean acidification from calcium isotopes in biogenic apatite.Crossref | GoogleScholarGoogle Scholar |
Izzo, C., Doubleday, Z., Schultz, A., Woodcock, S., and Gillanders, B. (2015). Contribution of water chemistry and fish condition to otolith chemistry: comparisons across salinity environments. Journal of Fish Biology 86, 1680–1698.
| Contribution of water chemistry and fish condition to otolith chemistry: comparisons across salinity environments.Crossref | GoogleScholarGoogle Scholar | 26033292PubMed |
Izzo, C., Doubleday, Z. A., Grammer, G. L., Gilmore, K. L., Alleway, H. K., Barnes, T. C., Disspain, M. C., Giraldo, A., Mazloumi, N., and Gillanders, B. M. (2016a). Fish as proxies of ecological and environmental change. Reviews in Fish Biology and Fisheries 26, 265–286.
| Fish as proxies of ecological and environmental change.Crossref | GoogleScholarGoogle Scholar |
Izzo, C., Huveneers, C., Drew, M., Bradshaw, C. J. A., Donnellan, S. C., and Gillanders, B. M. (2016b). Vertebral chemistry demonstrates movement and population structure of bronze whaler. Marine Ecology Progress Series 556, 195–207.
| Vertebral chemistry demonstrates movement and population structure of bronze whaler.Crossref | GoogleScholarGoogle Scholar |
Izzo, C., Reis‐Santos, P., and Gillanders, B. M. (2018). Otolith chemistry does not just reflect environmental conditions: a meta‐analytic evaluation. Fish and Fisheries 19, 441–454.
| Otolith chemistry does not just reflect environmental conditions: a meta‐analytic evaluation.Crossref | GoogleScholarGoogle Scholar |
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 |
Last, P., and Stevens, J. (2009). ‘Sharks and Rays of Australia’, 2nd edn. (CSIRO Publishing: Melbourne, Vic., Australia.)
Lefevre, S. (2016). Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction. Conservation Physiology 4, cow009.
| Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction.Crossref | GoogleScholarGoogle Scholar | 27766156PubMed |
Lewis, J. P., Patterson, W. F., Carlson, J. K., and McLachlin, K. (2016). Do vertebral chemical signatures distinguish juvenile blacktip shark (Carcharhinus limbatus) nursery regions in the northern Gulf of Mexico? Marine and Freshwater Research 67, 1014–1022.
| Do vertebral chemical signatures distinguish juvenile blacktip shark (Carcharhinus limbatus) nursery regions in the northern Gulf of Mexico?Crossref | GoogleScholarGoogle Scholar |
Lewis, J., Patterson, W., and Carlson, J. (2017). Natural variability and effects of cleaning and storage procedures on vertebral chemistry of the blacktip shark Carcharhinus limbatus. Journal of Fish Biology 91, 1284–1300.
| Natural variability and effects of cleaning and storage procedures on vertebral chemistry of the blacktip shark Carcharhinus limbatus.Crossref | GoogleScholarGoogle Scholar | 29023719PubMed |
Loewen, T. N., Carriere, B., Reist, J. D., Halden, N. M., and Anderson, W. G. (2016). Linking physiology and biomineralization processes to ecological inferences on the life history of fishes. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 202, 123–140.
| Linking physiology and biomineralization processes to ecological inferences on the life history of fishes.Crossref | GoogleScholarGoogle Scholar |
Martino, J., Doubleday, Z. A., Woodcock, S. H., and Gillanders, B. M. (2017). Elevated carbon dioxide and temperature affects otolith development, but not chemistry, in a diadromous fish. Journal of Experimental Marine Biology and Ecology 495, 57–64.
| Elevated carbon dioxide and temperature affects otolith development, but not chemistry, in a diadromous fish.Crossref | GoogleScholarGoogle Scholar |
McMillan, M. N., Izzo, C., Wade, B., and Gillanders, B. (2017a). Elements and elasmobranchs: hypotheses, assumptions and limitations of elemental analysis. Journal of Fish Biology 90, 559–594.
| Elements and elasmobranchs: hypotheses, assumptions and limitations of elemental analysis.Crossref | GoogleScholarGoogle Scholar | 27859234PubMed |
McMillan, M. N., Izzo, C., Junge, C., Albert, O., Jung, A., and Gillanders, B. M. (2017b). Analysis of vertebral chemistry to assess stock structure in a deep-sea shark, Etmopterus spinax. ICES Journal of Marine Science 74, 793–803.
| Analysis of vertebral chemistry to assess stock structure in a deep-sea shark, Etmopterus spinax.Crossref | GoogleScholarGoogle Scholar |
McMillan, M. N., Huveneers, C., Semmens, J. M., and Gillanders, B. M. (2018). Natural tags reveal populations of conservation dependent school shark use different pupping areas. Marine Ecology Progress Series 599, 147–156.
| Natural tags reveal populations of conservation dependent school shark use different pupping areas.Crossref | GoogleScholarGoogle Scholar |
McNeil, B. I., and Sasse, T. P. (2016). Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle. Nature 529, 383.
| Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle.Crossref | GoogleScholarGoogle Scholar | 26791726PubMed |
Miller, J. A. (2009). The effects of temperature and water concentration on the otolith incorporation of barium and manganese in black rockfish Sebastes melanops. Journal of Fish Biology 75, 39–60.
| The effects of temperature and water concentration on the otolith incorporation of barium and manganese in black rockfish Sebastes melanops.Crossref | GoogleScholarGoogle Scholar | 20738481PubMed |
Mirasole, A., Gillanders, B., Reis-Santos, P., Grassa, F., Capasso, G., Scopelliti, G., Mazzola, A., and Vizzini, S. (2017). The influence of high pCO2 on otolith shape, chemical and carbon isotope composition of six coastal fish species in a Mediterranean shallow CO2 vent. Marine Biology 164, 191.
| The influence of high pCO2 on otolith shape, chemical and carbon isotope composition of six coastal fish species in a Mediterranean shallow CO2 vent.Crossref | GoogleScholarGoogle Scholar |
Mohan, J. A., TinHan, T. C., Miller, N. R., and Wells, R. J. (2017). Effects of sample cleaning and storage on the elemental composition of shark vertebrae. Rapid Communications in Mass Spectrometry 31, 2073–2080.
| Effects of sample cleaning and storage on the elemental composition of shark vertebrae.Crossref | GoogleScholarGoogle Scholar | 28940897PubMed |
Mohan, J. A., Miller, N. R., Herzka, S. Z., Sosa-Nishizaki, O., Kohin, S., Dewar, H., Kinney, M., Snodgrass, O., and Wells, D. R. (2018). Elements of time and place: manganese and barium in shark vertebrae reflect age and upwelling histories. Proceedings of the Royal Society of London – B. Biological Sciences 285, 20181760.
| Elements of time and place: manganese and barium in shark vertebrae reflect age and upwelling histories.Crossref | GoogleScholarGoogle Scholar |
Morales-Nin, B. (2000). Review of the growth regulation processes of otolith daily increment formation. Fisheries Research 46, 53–67.
| Review of the growth regulation processes of otolith daily increment formation.Crossref | GoogleScholarGoogle Scholar |
Paton, C., Hellstrom, J., Paul, B., Woodhead, J., and Hergt, J. (2011). Iolite: freeware for the visualisation and processing of mass spectrometric data. Journal of Analytical Atomic Spectrometry 26, 2508–2518.
| Iolite: freeware for the visualisation and processing of mass spectrometric data.Crossref | GoogleScholarGoogle Scholar |
Pistevos, J. C., Nagelkerken, I., Rossi, T., Olmos, M., and Connell, S. D. (2015). Ocean acidification and global warming impair shark hunting behaviour and growth. Scientific Reports 5, 16293.
| Ocean acidification and global warming impair shark hunting behaviour and growth.Crossref | GoogleScholarGoogle Scholar | 26559327PubMed |
Pistevos, J. C., Nagelkerken, I., Rossi, T., and Connell, S. D. (2016). Antagonistic effects of ocean acidification and warming on hunting sharks. Oikos 126, 241–247.
| Antagonistic effects of ocean acidification and warming on hunting sharks.Crossref | GoogleScholarGoogle Scholar |
Radtke, R., and Shafer, D. (1992). Environmental sensitivity of fish otolith microchemistry. Marine and Freshwater Research 43, 935–951.
| Environmental sensitivity of fish otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Raoult, V., Howell, N., Zahra, D., Peddemors, V. M., Howard, D. L., de Jonge, M. D., Buchan, B. L., and Williamson, J. E. (2018). Localized zinc distribution in shark vertebrae suggests differential deposition during ontogeny and across vertebral structures. PLoS One 13, e0190927.
| Localized zinc distribution in shark vertebrae suggests differential deposition during ontogeny and across vertebral structures.Crossref | GoogleScholarGoogle Scholar | 29324879PubMed |
Reis‐Santos, P., Vasconcelos, R., Ruano, M., Latkoczy, C., Günther, D., Costa, M., and Cabral, H. (2008). Interspecific variations of otolith chemistry in estuarine fish nurseries. Journal of Fish Biology 72, 2595–2614.
| Interspecific variations of otolith chemistry in estuarine fish nurseries.Crossref | GoogleScholarGoogle Scholar |
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. Journal of Experimental Marine Biology and Ecology 446, 245–252.
| Effects of temperature, salinity and water composition on otolith elemental incorporation of Dicentrarchus labrax.Crossref | GoogleScholarGoogle Scholar |
Reis-Santos, P., Vasconcelos, R. P., Tanner, S. E., Fonseca, V. F., Cabral, H. N., and Gillanders, B. M. (2018). Extrinsic and intrinsic factors shape the ability of using otolith chemistry to characterise estuarine environmental histories. Marine Environmental Research 140, 332–341.
| Extrinsic and intrinsic factors shape the ability of using otolith chemistry to characterise estuarine environmental histories.Crossref | GoogleScholarGoogle Scholar | 30251648PubMed |
Ries, J. B., Cohen, A. L., and McCorkle, D. C. (2009). Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131–1134.
| Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification.Crossref | GoogleScholarGoogle Scholar |
Rodda, K., and Seymour, R. (2008). Functional morphology of embryonic development in the Port Jackson shark Heterodontus portusjacksoni (Meyer). Fish Biology 72, 961–984.
| Functional morphology of embryonic development in the Port Jackson shark Heterodontus portusjacksoni (Meyer).Crossref | GoogleScholarGoogle Scholar |
Rosa, R., Baptista, M., Lopes, V. M., Pegado, M., Paula, J., Trübenbach, K., Leal, M., Calado, R., and Repolho, T. (2014). Early-life exposure to climate change impairs tropical shark survival. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20141738.
| Early-life exposure to climate change impairs tropical shark survival.Crossref | GoogleScholarGoogle Scholar |
Smith, W. D. (2013). Vertebral elemental markers in elasmobranchs: potential for reconstructing environmental history and population structure. Ph.D. Thesis, Oregon State University, Corvallis, OR, USA.
Smith, W. D., Miller, J. A., and Heppell, S. S. (2013). Elemental markers in elasmobranchs: effects of environmental history and growth on vertebral chemistry. PLoS One 8, e62423.
| Elemental markers in elasmobranchs: effects of environmental history and growth on vertebral chemistry.Crossref | GoogleScholarGoogle Scholar | 24098320PubMed |
Smith, W. D., Miller, J. A., Márquez-Farías, J. F., and Heppell, S. S. (2016). Elemental signatures reveal the geographic origins of a highly migratory shark: prospects for measuring population connectivity. Marine Ecology Progress Series 556, 173–193.
| Elemental signatures reveal the geographic origins of a highly migratory shark: prospects for measuring population connectivity.Crossref | GoogleScholarGoogle Scholar |
Stanley, R. R., Bradbury, I. R., DiBacco, C., Snelgrove, P. V., Thorrold, S. R., and Killen, S. S. (2015). Environmentally mediated trends in otolith composition of juvenile Atlantic cod (Gadus morhua). ICES Journal of Marine Science 72, 2350–2363.
| Environmentally mediated trends in otolith composition of juvenile Atlantic cod (Gadus morhua).Crossref | GoogleScholarGoogle Scholar |
Sturrock, A., Trueman, C., Darnaude, A., and Hunter, E. (2012). Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? Journal of Fish Biology 81, 766–795.
| Can otolith elemental chemistry retrospectively track migrations in fully marine fishes?Crossref | GoogleScholarGoogle Scholar | 22803735PubMed |
Sturrock, A. M., Trueman, C. N., Milton, J. A., Waring, C. P., Cooper, M. J., and Hunter, E. (2014). Physiological influences can outweigh environmental signals in otolith microchemistry research. Marine Ecology Progress Series 500, 245–264.
| Physiological influences can outweigh environmental signals in otolith microchemistry research.Crossref | GoogleScholarGoogle Scholar |
Sturrock, A., Hunter, E., Milton, A. J., 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 |
Thomas, O. R., Ganio, K., Roberts, B. R., and Swearer, S. E. (2017). Trace element–protein interactions in endolymph from the inner ear of fish: implications for environmental reconstructions using fish otolith chemistry. Metallomics 9, 239–249.
| Trace element–protein interactions in endolymph from the inner ear of fish: implications for environmental reconstructions using fish otolith chemistry.Crossref | GoogleScholarGoogle Scholar | 28091665PubMed |
Tillett, B., Meekan, M., Parry, D., Munksgaard, N., Field, I., Thorburn, D., and Bradshaw, C. (2011). Decoding fingerprints: elemental composition of vertebrae correlates to age-related habitat use in two morphologically similar sharks. Marine Ecology Progress Series 434, 133–142.
| Decoding fingerprints: elemental composition of vertebrae correlates to age-related habitat use in two morphologically similar sharks.Crossref | GoogleScholarGoogle Scholar |
Tzadik, O. E., Curtis, J. S., Granneman, J. E., Kurth, B. N., Pusack, T. J., Wallace, A. A., Hollander, D. J., Peebles, E. B., and Stallings, C. D. (2017). Chemical archives in fishes beyond otoliths: a review on the use of other body parts as chronological recorders of microchemical constituents for expanding interpretations of environmental, ecological, and life-history changes. Limnology and Oceanography, Methods 15, 238–263.
| Chemical archives in fishes beyond otoliths: a review on the use of other body parts as chronological recorders of microchemical constituents for expanding interpretations of environmental, ecological, and life-history changes.Crossref | GoogleScholarGoogle Scholar |
Walther, B. D. (2019). The art of otolith chemistry: interpreting patterns by integrating perspectives. Marine and Freshwater Research , .
| The art of otolith chemistry: interpreting patterns by integrating perspectives.Crossref | GoogleScholarGoogle Scholar |
Walther, B., and Thorrold, S. (2006). Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Marine Ecology Progress Series 311, 125–130.
| Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish.Crossref | GoogleScholarGoogle Scholar |
Watanabe, T., Kiron, V., and Satoh, S. (1997). Trace minerals in fish nutrition. Aquaculture 151, 185–207.
| Trace minerals in fish nutrition.Crossref | GoogleScholarGoogle Scholar |
Webb, S., Woodcock, S., and Gillanders, B. (2012). Sources of otolith barium and strontium in estuarine fish and the influence of salinity and temperature. Marine Ecology Progress Series 453, 189–199.
| Sources of otolith barium and strontium in estuarine fish and the influence of salinity and temperature.Crossref | GoogleScholarGoogle Scholar |
Werry, J., Lee, S., Otway, N., Hu, Y., and Sumpton, W. (2011). A multi-faceted approach for quantifying the estuarine–nearshore transition in the life cycle of the bull shark, Carcharhinus leucas. Marine and Freshwater Research 62, 1421–1431.
| A multi-faceted approach for quantifying the estuarine–nearshore transition in the life cycle of the bull shark, Carcharhinus leucas.Crossref | GoogleScholarGoogle Scholar |
Wood, H. L., Spicer, J. I., and Widdicombe, S. (2008). Ocean acidification may increase calcification rates, but at a cost. Proceedings of the Royal Society of London – B. Biological Sciences 275, 1767–1773.
| Ocean acidification may increase calcification rates, but at a cost.Crossref | GoogleScholarGoogle Scholar |
