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Ontogenetic patterns in the calcification and element incorporation in fin rays of age-0 White Sturgeon

Abstract

White Sturgeon (Acipenser transmontanus) are a long-lived, slow-growing, and late-reproducing anadromous fish common in estuaries and coastal habitats along the North American West Coast. These life history characteristics make populations vulnerable to human impacts and a challenge to study and manage. Previous studies in the San Francisco Estuary, California have provided insights into rearing habitats and migratory patterns but are limited in spatial and temporal scope. Fin ray geochemical analysis can provide a non-lethal approach to reconstruct migratory patterns and environmental conditions experienced throughout an individual fish’s lifespan. However, it is not known how soon post hatch age-0 White Sturgeon fin rays begin to calcify, reducing confidence in early life history temporal resolution using geochemical approaches. We used osteological (clear and stain) and geochemical techniques (laser-ablation-ICP-MS) to describe calcification initiation and completion, and element incorporation in the leading fin ray of known-age White Sturgeon reared at constant water temperature (18.6 °C) from 1 to 76 days post hatch (dph). We found that fin rays begin calcifying as early as ~20 dph (~27 mm total length) and are >95% calcified by ~72 dph (~70 mm total length). Consequently, the first ~20 dph are not likely to be recorded in the fin ray. Observed element (Li, Mg, Cu, Zn, Rb, Sr, Ba, Pb, U) incorporation patterns suggest that fin rays can provide a powerful tool to study White Sturgeon early movement and migratory patterns, habitat use, and environmental exposure.

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References

  • Allan RP, Soden BJ (2008) Atmospheric warming and the amplification of precipitation extremes. Science 321:1481–1484. https://doi.org/10.1126/science.1160787

    CAS  Article  PubMed  Google Scholar 

  • Allen PJ, Hobbs JA, Cech JJ et al (2009a) Using trace elements in pectoral fin rays to assess life history movements in sturgeon: estimating age at initial seawater entry in Klamath River green sturgeon. Trans Am Fish Soc 138:240–250. https://doi.org/10.1577/t08-061.1

    CAS  Article  Google Scholar 

  • Allen PJ, Webb MAHH, Cureton E et al (2009b) Calcium regulation in wild populations of a freshwater cartilaginous fish, the lake sturgeon Acipenser fulvescens. Comp Biochem Physiol Part A Mol Integr Physiol 154:437–450. https://doi.org/10.1016/j.cbpa.2009.07.014

    CAS  Article  Google Scholar 

  • Allen PJ, Baumgartner W, Brinkman E, DeVries RJ, Stewart HA, Aboagye DL, Ramee SW, Ciaramella MA, Culpepper CM III, Petrie-Hanson L (2018) Fin healing and regeneration in sturgeon. J Fish Biol 93:917–930. https://doi.org/10.1111/jfb.13794

    CAS  Article  PubMed  Google Scholar 

  • Arai T, Levin AV, Boltunov AN, Miyazaki N (2002) Migratory historyof the Russian sturgeon Acipenser guldenstadti in the Caspian Sea, as revealed by pectoral fin spine Sr: Ca ratios. Mar Biol 141:315–319

    Article  Google Scholar 

  • Avigliano E, Saez MB, Rico R, Volpedo AV (2015a) Use of otolith strontium:calcium and zinc:calcium ratios as an indicator of the habitat of Percophis brasiliensis Quoy & Gaimard, 1825 in the southwestern Atlantic Ocean. Neotrop Ichthyol 13:187–194. https://doi.org/10.1590/1982-0224-20130235

    Article  Google Scholar 

  • Avigliano E, Schenone NF, Volpedo AV, Goessler W, Fernández Cirelli A (2015b) Heavy metals and trace elements in muscle of silverside (Odontesthes bonariensis) and water from different environments (Argentina): aquatic pollution and consumption effect approach. Sci Total Environ 506–507:102–108. https://doi.org/10.1016/j.scitotenv.2014.10.119

    CAS  Article  PubMed  Google Scholar 

  • Ay Ö, Kalay M, Tamer L, Canli M (1999) Copper and lead accumulation in tissues of a freshwater fish Tilapia zillii and its effects on the branchial Na,K-ATPase activity. Bull Environ Contam Toxicol 62:160–168. https://doi.org/10.1007/s001289900855

    CAS  Article  PubMed  Google Scholar 

  • Barnett PR, Mallory EC (1971) Determination of minor elements in water by emission spectroscopy. Tech Water-Resources Investig USGS Publ:05–A2

  • Barnett-Johnson R, Pearson TE, Ramos FC et al (2008) Tracking natal origins of salmon using isotopes, otoliths, and landscape geology. Limnol Oceanogr 53:1633–1642. https://doi.org/10.4319/lo.2008.53.4.1633

    CAS  Article  Google Scholar 

  • Beamish RJ (1981) Use of fin-ray sections to age walleye Pollock, Pacific cod, and albacore, and the importance of this method. Trans Am Fish Soc 110:287–299. https://doi.org/10.1577/1548-8659(1981)110<287:uofsta>2.0.co;2

    Article  Google Scholar 

  • Beamish RJ, Chilton D (1977) Age determination of lingcod (Ophiodon elongatus) using dorsal fin rays and scales. J Fish Res Board Canada 34:1305–1313. https://doi.org/10.1139/f77-192

    Article  Google Scholar 

  • Birstein VJ (1993) Sturgeons and paddlefishes: threatened fishes in need of conservation. Conserv Biol 7:773–787. https://doi.org/10.1046/j.1523-1739.1993.740773.x

    Article  Google Scholar 

  • Birstein VJ, Waldman JR, Bemis WE (2006) Sturgeon biodiversity and conservation. Springer Sci Bus Media 17

  • Blumenthal NC (1990) The in vitro and in vivo uptake of trace elements by hydroxyapatite. In: Priest ND, Van de Vyver FL (eds) Trace metals and fluoride in bones and teeth. CRC Press, Boca Raton, Florida, pp 307–313

    Google Scholar 

  • Boreman J (1997) Sensitivity of north American sturgeons and paddlefish to fishing mortality. Environ Biol Fish 48:399–405. https://doi.org/10.1007/0-306-46854-9_28

    Article  Google Scholar 

  • Brennan JS, Cailliet GM (1989) Comparative age-determination techniques for white sturgeon in California. Trans Am Fish Soc 118:296–310. https://doi.org/10.1577/1548-8659(1989)118<0296

    Article  Google Scholar 

  • Campana SE (1999) Chemistry and composition of fish otoliths: pathways,mechanisms and applications. Mar Ecol 188:263–297

    CAS  Article  Google Scholar 

  • Cech JJ, Mitchell SJ, Wragg TE (1984) Comparative growth of juvenile white sturgeon and striped bass: effects of temperature and hypoxia. Estuaries 7:12–18

    Article  Google Scholar 

  • Clarke AD, Telmer KH, Mark Shrimpton J (2007) Elemental analysis of otoliths, fin rays and scales: a comparison of bony structures to provide population and life-history information for the Arctic grayling (Thymallus arcticus). Ecol Freshw Fish 16:354–361. https://doi.org/10.1111/j.1600-0633.2007.00232.x

    Article  Google Scholar 

  • Collins MR, Smith TIJ (1996) Sturgeon fin ray removal is nondeleterious. N Am J Fish Manag 16:939–941

    Article  Google Scholar 

  • Counihan TD, Chapman CG (2018) Relating river discharge and water temperature to the recruitment of age-0 white sturgeon (Acipenser transmontanus Richardson, 1836) in the Columbia River using over-dispersed catch data. J Appl Ichthyol 34:279–289. https://doi.org/10.1111/jai.13570

    Article  Google Scholar 

  • Deng D-F, Koshio S, Yokoyama S, Bai SC, Shao Q, Cui Y, Hung SSO (2003) Effects of feeding rate on growth performance of white sturgeon (Acipenser transmontanus) larvae. Aquaculture 217:589–598. https://doi.org/10.1016/S0044-8486(02)00461-1

    Article  Google Scholar 

  • Dettinger M (2011) Climate change, atmospheric rivers, and floods in California-a multimodel analysis of storm frequency and magnitude changes. J Am Water Resour Assoc 47:514–523. https://doi.org/10.1111/j.1752-1688.2011.00546.x

    Article  Google Scholar 

  • Dillman CB, Hilton EJ (2015) Anatomy and early development of the pectoral girdle, fin, and fin spine of sturgeons (Actinopterygii: Acipenseridae): anatomy and early development. J Morphol 276:241–260. https://doi.org/10.1002/jmor.20328

    Article  PubMed  Google Scholar 

  • Dingerkus G, Uhler LD (1977) Enzyme clearing of Alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol 52:229–232. https://doi.org/10.3109/10520297709116780

    CAS  Article  PubMed  Google Scholar 

  • Ellis NA, Miller CT (2016) Dissection and flat-mounting of the Threespine stickleback Branchial skeleton. J Vis Exp:1–7. https://doi.org/10.3791/54056

  • Eshaghzadeh H, Akbarzadeh A, Yarmohammadi M, Gisbert E (2018) Skeletogenesis in the Persian sturgeon Acipenser persicus and its correlation with gene expression of vitamin K-dependent proteins during larval development: skeletogenesis in a. persicus. J Fish Biol 92:452–469. https://doi.org/10.1111/jfb.13527

    CAS  Article  PubMed  Google Scholar 

  • Feyrer F, Hobbs JA, Baerwald M, Sommer T, Yin QZ, Clark K, May B, Bennett W (2007) Otolith microchemistry provides information complementary to microsatellite DNA for a migratory fish. Trans Am Fish Soc 136:469–476. https://doi.org/10.1577/T06-044.1

    CAS  Article  Google Scholar 

  • Faukner JR, Jackson ZJ (2014) 2013 San Joaquin river white sturgeon telemetry study. Stockton Fish and wildlife office, anadromous fish restoration program, U. S. Fish and wildlife Service, Lodi, California

  • Gillanders BM (2001) Trace metals in four structures of fish and their use for estimates of stock structure. Fish Bull 99:410–419

    Google Scholar 

  • Gundersen DT, Zeug SC, Bringolf RB, Merz J, Jackson Z, Webb MAH (2017) Tissue contaminant burdens in San Francisco estuary white sturgeon (Acipenser transmontanus): implications for population recovery. Arch Environ Contam Toxicol 73:334–347. https://doi.org/10.1007/s00244-017-0378-9

    CAS  Article  PubMed  Google Scholar 

  • Hatten JR, Parsley MJ, Barton GJ, Batt TR, Fosness RL (2018) Substrate and flow characteristics associated with white sturgeon recruitment in the Columbia River basin. Heliyon 4:e00629. https://doi.org/10.1016/j.heliyon.2018.e00629

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Helfman GS, Collette BB, Facey DE, Bowen BW (1997) The diversity of fishes. Blackwell Science, Malden, Massachuetts

  • Heublein J, Bellmer R, Chase RD et al (2017) Life history and current monitoring inventory of San Francisco estuary sturgeon. NOAA Tech Memo NMFS. https://doi.org/10.7289/V5/TM-SWFSC-589

  • Hildebrand LR, Drauch Schreier A, Lepla K, McAdam SO, McLellan J, Parsley MJ, Paragamian VL, Young SP (2016) Status of white sturgeon ( Acipenser transmontanus Richardson, 1863) throughout the species range, threats to survival, and prognosis for the future. J Appl Ichthyol 32:261–312. https://doi.org/10.1111/jai.13243

    Article  Google Scholar 

  • Hobbs JA, Yin Q, Burton J, Bennett WA (2005) Retrospective determination of natal habitats for an estuarine fish with otolith strontium isotope ratios. Mar Freshw Res 56:655. https://doi.org/10.1071/MF04136

    CAS  Article  Google Scholar 

  • Hobbs JA, Lewis LS, Ikemiyagi N, Sommer T, Baxter RD (2010) The use of otolith strontium isotopes (87Sr/86Sr) to identify nursery habitat for a threatened estuarine fish. Environ Biol Fish 89:557–569. https://doi.org/10.1007/s10641-010-9672-3

    Article  Google Scholar 

  • Hobbs JA, Lewis LS, Willmes M, Denney C, Bush E (2019) Complex life histories discovered in a critically endangered fish. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-52273-8

    CAS  Article  Google Scholar 

  • Hüssy K, Limburg KE, de Pontual H, Thomas ORB, Cook PK, Heimbrand Y, Blass M, Sturrock AM (2020) Trace element patterns in Otoliths: the role of biomineralization. Rev Fish Sci Aquac 0:1–33. https://doi.org/10.1080/23308249.2020.1760204

  • Israel JA, Drauch A, Gingras M (2009) Life history conceptual model, white sturgeon (Acipenser transmontanus). Delta regional Ecosyetem restoration implementation plan. Sacramento, Ca

    Google Scholar 

  • Jackson ZJ, Gruber JJ, Van Eenennaam JP (2016) White sturgeon spawning in the San Joaquin River, California, and effects of water management. J Fish Wildl Manag 7:171–180. https://doi.org/10.3996/092015-jfwm-092

    Article  Google Scholar 

  • 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 Geoanalytical Res 35:397–429. https://doi.org/10.1111/j.1751-908X.2011.00120.x

    CAS  Article  Google Scholar 

  • Kalay M, Ay Ö, Canli M (1999) Heavy metal concentrations in fish tissues from the Northeast Mediterranean Sea. Bull Environ Contam Toxicol 63:673–681

    CAS  Article  Google Scholar 

  • Kalish JM (1991) Determinants of otolith chemistry: seasonal variation in the composition of blood plasma, endolymph and otoliths of bearded rock cod Pseudophysis barbatus. Mar Ecol Prog Ser 74:137–159

    CAS  Article  Google Scholar 

  • Kerr LA, Campana SE (2014) Chemical composition of fish hard parts as a natural marker of fish stocks. In: Stock identification methods, 2nd edn. Academic Press, San Diego, pp 205–234

    Chapter  Google Scholar 

  • Klimley AP, Chapman ED, Cech JJ, et al (2015) Sturgeon in the Sacramento–San Joaquin Watershed: new insights to support conservation and management. San Fr Estuary Watershed Sci 13. https://doi.org/10.15447/sfews.2015v13iss4art1

  • Kohlhorst DW, Cech JJ (2001) White sturgeon. California’s living mar resour a status report Calif Dep Fish Game 467–469

  • Kohlhorst DW, Botsford LW, Brennan JS, Cailliet GM (1991) Aspects of the structure and dynamics of an exploited Central California population of white sturgeon (Acipenser transmontanus). 1st Int Symp Sturgeon 277–293

  • Lee S, Fadel JG, Haller LY, Verhille CE, Fangue NA, Hung SSO (2015) Effects of feed restriction on salinity tolerance in white sturgeon (Acipenser transmontanus). Comp Biochem Physiol Part A Mol Integr Physiol 188:156–167. https://doi.org/10.1016/j.cbpa.2015.06.027

    CAS  Article  Google Scholar 

  • Longerich HP, Jackson SE, Günther D (1996) Laser ablation inductively coupled plasma mass spectrometric transient signal data acquisition and analyte concentration calculation. J Anal At Spectrom 11:899–904. https://doi.org/10.1039/Ja9961100899

    CAS  Article  Google Scholar 

  • McAdam SO (2011) Effects of substrate condition on habitat use and survival by white sturgeon (Acipenser transmontanus) larvae and potential implications for recruitment. Can J Fish Aquat Sci 68:812–822. https://doi.org/10.1139/f2011-021

    Article  Google Scholar 

  • Melancon S, Fryer BJ, Ludsin SA, Gagnon JE, Yang Z (2005) Effects of crystal structure on the uptake of metals by lake trout (Salvelinus namaycush) otoliths. Can J Fish Aquat Sci 62:2609–2619. https://doi.org/10.1139/f05-161

    CAS  Article  Google Scholar 

  • Miller EA, Singer GP, Peterson ML, Chapman ED, Johnston ME, Thomas MJ, Battleson RD, Gingras M, Klimley AP (2020) Spatio-temporal distribution of green sturgeon (Acipenser medirostris) and white sturgeon (a. transmontanus) in the San Francisco estuary and Sacramento River, California. Environ Biol Fish 103:577–603. https://doi.org/10.1007/s10641-020-00972-x

    Article  Google Scholar 

  • Moyle PB (2002) Inland fishes of California. University of California Press, Berkeley

    Google Scholar 

  • Müller W, Anczkiewicz R (2016) Accuracy of laser-ablation (LA)-MC-ICPMS Sr isotope analysis of (bio)apatite-a problem reassessed. J Anal At Spectrom 31:259–269. https://doi.org/10.1039/c5ja00311c

    Article  Google Scholar 

  • Mytton GR, Jessee ZJ, Heironimus LB, et al (2018) 2016 San Joaquin River sturgeon spawning survey. Lodi fish and wildlife office, anadromous fish restoration program, U.S. Fish and Wildlife Service, Lodi, California

  • Nelson TC, Doukakis P, Lindley ST, Schreier AD, Hightower JE, Hildebrand LR, Whitlock RE, Webb MAH (2013) Research tools to investigate movements, migrations, and life history of sturgeons (Acipenseridae), with an emphasis on marine-oriented populations. PLoS One 8:e71552. https://doi.org/10.1371/journal.pone.0071552

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen PL, Jackson ZJ, Peterson DL (2016) Comparison of fin ray sampling methods on white sturgeon Acipenser transmontanus growth and swimming performance. J Fish Bio 88:655–667

    CAS  Article  Google Scholar 

  • Paton C, Hellstrom J, Paul B, Woodhead J, Hergt J (2011) Iolite: freeware for the visualization and processing of mass spectrometric data. J Anal At Spectrom 26:2508

    CAS  Article  Google Scholar 

  • Phelps QE, Whitledge GW, Tripp SJ, Smith KT, Garvey JE, Herzog DP, Ostendorf DE, Ridings JW, Crites JW, Hrabik RA, Doyle WJ, Hill TD (2012) Identifying river of origin for age-0 Scaphirhynchus sturgeons in the Missouri and Mississippi rivers using fin ray microchemistry. Can J Fish Aquat Sci 69:930–941. https://doi.org/10.1139/f2012-038

    CAS  Article  Google Scholar 

  • Phelps QE, Hupfeld RN, Whitledge GW (2017) Lake sturgeon Acipenser fulvescens and shovelnose sturgeon Scaphirhynchus platorynchus environmental life history revealed using pectoral fin-ray microchemistry: implications for interjurisdictional conservation through fishery closure zones. J Fish Biol 90:626–639. https://doi.org/10.1111/jfb.13242

    CAS  Article  PubMed  Google Scholar 

  • Pracheil BM, Chakoumakos BC, Feygenson ML, Whitledge GW, Koenigs RP, Bruch RM (2016) Sturgeon and paddlefish (Acipenseridae) sagittal otoliths are composed of the calcium carbonate polymorphs vaterite and calcite: acipenseridae otoliths are vaterite and calcite. J Fish Biol 90:549–558. https://doi.org/10.1111/jfb.13085

    Article  PubMed  Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing

  • Rien TA, Beamesderfer RCP (1994) Accuracy and precision of white sturgeon age estimates from pectoral fin rays. Trans Am Fish Soc 123:255–265. https://doi.org/10.1577/1548-8659(1994)123<0255:AAPOWS>2.3.CO;2

    Article  Google Scholar 

  • Rodgers EM, Todgham AE, Connon RE, Fangue NA (2018) Stressor interactions in freshwater habitats: effects of cold water exposure and food limitation on early-life growth and upper thermal tolerance in white sturgeon, Acipenser transmontanus. Freshw Biol 64:348–358. https://doi.org/10.1111/fwb.13224

    Article  Google Scholar 

  • Rude NP, Smith KT, Whitledge GW (2014) Identification of stocked muskellunge and potential for distinguishing hatchery-origin and wild fish using pelvic fin ray microchemistry. Fish Manag Ecol 21:312–321. https://doi.org/10.1111/fme.12081

    Article  Google Scholar 

  • Sellheim K, Willmes M, Hobbs JA, Glessner JJG, Jackson ZJ, Merz JE (2017) Validating fin ray microchemistry as a tool to reconstruct the migratory history of white sturgeon. Trans Am Fish Soc 146:844–857. https://doi.org/10.1080/00028487.2017.1320305

    Article  Google Scholar 

  • Skinner JE (1962) An historical review of the fish and wildlife resources of the San Francisco Bay area. Calif Dept Fish Game, Water Proj Br. Rept. 1, 226p

  • Smith SE, Kato S (1979) The fisheries of San Francisco Bay: past, present, and future. Golden Gate Park, San Francisco CA

    Google Scholar 

  • Stavri S, Zarnescu O (2013) The expression of alkaline phosphatase, Osteopontin, Osteocalcin, and chondroitin sulfate during pectoral fin regeneration in Carassius Auratus Gibelio: a combined Histochemical and Immunohistochemical study. Microsc Microanal 19:91–95

    Article  Google Scholar 

  • Stevens DE, Miller LW (1970) Distribution of sturgeon larvae in the Sacramento-San Joaquin River system. Calif Dep Fish Game 56:80–86

    Google Scholar 

  • Stevenson JT, Secor DH (2000) Age determination and growth of Hudson River Atlantic sturgeon, Acipenser oxyrinchus. Fish Bull 98:153–166

    Google Scholar 

  • Sturrock AM, Trueman CN, Darnaude AM, Hunter E (2012) Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? J Fish Biol 81:766–795. https://doi.org/10.1111/j.1095-8649.2012.03372.x

    CAS  Article  PubMed  Google Scholar 

  • Sturrock AM, Hunter E, Milton JA, EIMF, Johnson RC, Waring CP, Trueman CN (2015) Quantifying physiological influences on otolith microchemistry. Methods Ecol Evol 6:806–816. https://doi.org/10.1111/2041-210X.12381

    Article  Google Scholar 

  • Taylor WR, Van Dyke GC (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cymbium 9:107–119

    Google Scholar 

  • Tzadik OE, Curtis JS, Granneman JE, Kurth BN, Pusack TJ, Wallace AA, Hollander DJ, Peebles EB, Stallings CD (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. Limnol Oceanogr Methods 15:238–263. https://doi.org/10.1002/lom3.10153

    CAS  Article  Google Scholar 

  • Ugarte A, Abrego Z, Unceta N, Goicolea MA, Barrio RJ (2012) Evaluation of the bioaccumulation of trace elements in tuna species by correlation analysis between their concentrations in muscle and first dorsal spine using microwave-assisted digestion and ICP-MS. Int J Environ Anal Chem 92:1761–1775. https://doi.org/10.1080/03067319.2011.603078

    CAS  Article  Google Scholar 

  • Veinott GI, Evans RD (1999) An examination of elemental stability in the fin ray of the white sturgeon with laser ablation sampling – inductively coupled plasma – mass an examination of elemental stability in the fin ray of the. Trans Am Fish Soc 128:37–41. https://doi.org/10.1577/1548-8659(1999)128<0352

    Article  Google Scholar 

  • Veinott GI, Northcote T, Rosenau M, Evans RD (1999) Concentrations of strontium in the pectoral fin rays of the white sturgeon (Acipenser transmontanus) by laser ablation sampling – inductively coupled plasma – mass spectrometry as an indicator of marine migrations. Can J Fish Aquat Sci 56:10

    Article  Google Scholar 

  • Verhille CE, Poletto JB, Cocherell DE et al (2014) Larval green and white sturgeon swimming performance in relation to water-diversion flows. Conserv Physiol 2:cou031–cou031. https://doi.org/10.1093/conphys/cou031

  • Vroon PZ, Van Der Wagt B, Koornneef JM, Davies GR (2008) Problems in obtaining precise and accurate Sr isotope analysis from geological materials using laser ablation MC-ICPMS. Anal Bioanal Chem 390:465–476. https://doi.org/10.1007/s00216-007-1742-9

    CAS  Article  PubMed  Google Scholar 

  • Walker MB, Kimmel CB (2007) A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 82:23–28. https://doi.org/10.1080/10520290701333558

    CAS  Article  PubMed  Google Scholar 

  • Walther BD, Thorrold SR (2006) Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Mar Ecol Prog Ser 311:125–130

    CAS  Article  Google Scholar 

  • Wang JC (1986) Fishes of the Sacramento-San Joaquin estuary and adjacent waters. A guide to the early life histories, California

    Google Scholar 

  • Ward DM, Nislow KH, Chen CY, Folt CL (2010) Reduced trace element concentrations in fast-growing juvenile Atlantic Salmon in natural streams. Environ Sci Technol 44:3245–3251. https://doi.org/10.1021/es902639a

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wassersug RJ (1976) A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Stain Technol 51:131–134. https://doi.org/10.3109/10520297609116684

    CAS  Article  PubMed  Google Scholar 

  • Wells BK, Rieman BE, Clayton JL, Horan DL, Jones CM (2003) Relationships between water, Otolith, and scale chemistries of Westslope cutthroat trout from the Coeur d’Alene River, Idaho: the potential application of hard-part chemistry to describe movements in freshwater. Trans Am Fish Soc 132:409–424. https://doi.org/10.1577/1548-8659(2003)132<0409:rbwoas>2.0.co;2

    CAS  Article  Google Scholar 

  • Williams DR (1971) The metals of life. Van Nostrand Reinhold Company, London

    Google Scholar 

  • Willmes M, Glessner JJG, Carleton SA, Gerrity PC, Hobbs JA (2016) 87Sr/86Sr isotope ratio analysis by laser ablation MC-ICP-MS in scales, spines, and fin rays as a nonlethal alternative to otoliths for reconstructing fish life history. Can J Fish Aquat Sci 73:1852–1860. https://doi.org/10.1139/cjfas-2016-0103

    CAS  Article  Google Scholar 

  • Woodhead J, Swearer S, Hergt J, Maas R (2005) In situ Sr-isotope analysis of carbonates by LA-MC-ICP-MS: interference corrections, high spatial resolution and an example from otolith studies. J Anal At Spectrom 20:22–27. https://doi.org/10.1039/b412730g

    CAS  Article  Google Scholar 

  • Zarri LJ, Mehl SB, Palkovacs EP, Fangue NA (2019) Key transitions in morphological development improve age estimates in white sturgeon Acipenser transmontanus. J Fish Biol 94:815–819. https://doi.org/10.1111/jfb.13954

    Article  PubMed  Google Scholar 

  • Zheng KK, Deng D-F, De Riu N et al (2015) The effect of feeding rate on the growth performance of green sturgeon (Acipenser medirostris) fry. Aquac Nutr 21:489–495. https://doi.org/10.1016/S0044-8486(02)00461-1

    CAS  Article  Google Scholar 

  • Zimmerman CE (2005) Relationship of otolith strontium-to-calcium ratios and salinity: experimental validation for juvenile salmonids. Can J Fish Aquat Sci 62:88–97. https://doi.org/10.1139/f04-182

    CAS  Article  Google Scholar 

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Acknowledgements

U.S. Fish and Wildlife Service Anadromous Fish Restoration Program (USFWS AFRP) funded this project (Grant #F11AC01162 and #F16AC01081-02). The UC Davis Agricultural Experiment Station (grant #2098-H) to NAF and the UC Davis Animal Biology Graduate Group fellowship also provided funding support. Fish husbandry was performed at the UC Davis CABA facility under IACUC protocol #1867. CABA facility staff, Fangue Laboratory staff and Todgham laboratory staff at UC Davis, especially S. Baird and D. Cocherell, provided experimental juvenile White Sturgeon and laboratory space. L. Zarri, K. Karpenko and J. Shen assisted with sample collection and data entry. The Wainwright laboratory at UC Davis, especially P. Wainwright and M. Rupp provided valuable information on clear and stain methods. H. Spero (Stable Isotope laboratory in the UC Davis Department of Earth and Planetary Sciences) provided laboratory space to process fin rays where elemental chemistry was conducted. J. Glessner and A. Cole (UC Davis Interdisciplinary Center for Plasma Mass Spectrometry) processed water samples. T. Hinkelman provided assistance and guidance with statistical analysis. Z. Jackson (USFWS), J. Glessner (UC Davis) and J. Cech (UC Davis) provided thoughtful comments and valuable feedback throughout the writing process. Finally, we would like to thank Jan-Michael Hessenauer and two anonymous reviewers who provided valuable suggestions and comments in the review of this manuscript.

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Sweeney, J.K., Willmes, M., Sellheim, K. et al. Ontogenetic patterns in the calcification and element incorporation in fin rays of age-0 White Sturgeon. Environ Biol Fish 103, 1401–1418 (2020). https://doi.org/10.1007/s10641-020-01031-1

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  • DOI: https://doi.org/10.1007/s10641-020-01031-1

Keywords

  • Acipenser transmontanus
  • Fin ray
  • Microchemistry
  • Laser-ablation
  • Early development
  • Rearing