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Sturgeon and Paddlefish (Acipenseridae) Saggital Otoliths Are Composed of the Calcium Carbonate Polymorphs Vaterite and Calcite

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Sturgeon and Paddlefish (Acipenseridae) Saggital Otoliths Are Composed of the Calcium Carbonate Polymorphs Vaterite and Calcite Journal of Fish Biology (2016) doi:10.1111/jfb.13085, available online at wileyonlinelibrary.com Sturgeon and paddlefish (Acipenseridae) saggital otoliths are composed of the calcium carbonate polymorphs vaterite and calcite B. M. Pracheil*†, B. C. Chakoumakos‡, M. Feygenson§, G. W. Whitledge‖, R. P. Koenigs¶ and R. M. Bruch¶ *Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A., ‡Quantum Condensed Matter Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A., §Chemical and Engineering Materials Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A., ‖Center for Fisheries, Aquaculture and Aquatic Sciences, Southern Illinois University, Carbondale, IL 62901, U.S.A. and ¶Wisconsin Department of Natural Resources, Oshkosh, WI 54903, U.S.A. This study sought to resolve whether sturgeon (Acipenseridae) sagittae (otoliths) contain a non-vaterite fraction and to quantify how large a non-vaterite fraction is using neutron diffraction analysis. This study found that all otoliths examined had a calcite fraction that ranged from 18 ± 6to36± 3% by mass. This calcite fraction is most probably due to biological variation during otolith formation rather than an artefact of polymorph transformation during preparation. © 2016 The Fisheries Society of the British Isles Key words: Acipenser fulvescens. Otoliths, the calcium carbonate (CaCO3) ear bones of Osteichthyes, are truly a wonder of the Animal Kingdom. These tri-part structures essential for hearing and balance in fishes are composed of some form of3 CaCO and can be used to determine fish environmental history as well as fish age through enumeration of daily and annular rings (Pracheil et al., 2014). The three most common forms, or polymorphs, of CaCO3 are vaterite, which is the least energetically stable, intermediately stable aragonite and the most stable, calcite. All have all been reported from fish otoliths (Gauldie, 1993; Oliveira et al., 1996; Melancon et al., 2005). The polymorph or polymorphs of CaCO3 contained in the otolith of a particular fish species has been reported to reflect some phylogenetic patterning, with vaterite being the primary constituent of otoliths in the most primitive fishes and aragonite being the primary constituent of otoliths inmore modern fishes (Carlström, 1963; Gauldie, 1993). Despite its thermodynamic favourability and its dominance in the otoliths of land animals (Carlström, 1963), otoliths of only a few fishes have been reported to contain the most stable CaCO3 polymorph, calcite. Piranhas (Characiformes), hake (Gadi- formes), orange roughy (Beryciformes) and snapper (Perciformes), for example, have †Author to whom correspondence should be addressed. Tel.: +1 865 241 5622; email: [email protected] 1 © 2016 The Fisheries Society of the British Isles 2 B. M. PRACHEIL ET AL. been reported to contain otoliths made of all three polymorphs of CaCO3 (Gauldie, 1993; Oliveira et al., 1996). Previous reports have described sturgeon otoliths as being entirely composed of vaterite, although there was mention of small calcite and aragonite fractions that were potentially an artifact of preservation (Carlström, 1963; Gauldie, 1993). The mechanism that might lead to a preservation-induced polymorph transition, however, is not clear. The coexistence of multiple polymorphs in a single otolith has been reported from other fishes, but polymorph composition is controlled by proteins involved in otolith formation (Söllner et al., 2003; Tohse et al., 2009; Ren et al., 2013) rather than transformation of polymorphs post-nucleation. When taken together, this suggests the possibility of sturgeon otoliths actually containing fractions of other polymorphs. There have been some reports of visible differences among CaCO3 polymorphs observed using light microscopy (Gauldie, 1986; Bowen et al., 1999; Tomás & Geffen, 2003; Tomás et al., 2004); reliable visual determination among polymorphs, however, has not been quantitatively demonstrated. Rather, methods for polymorph determina- tion must rely on scattering techniques for determining the crystallographic structure of the CaCO3, e.g. powder diffraction or Raman spectroscopy. Earlier studies of otolith polymorph composition have used X-ray diffraction (Carlström, 1963; Gauldie, 1993; Oliveira et al., 1996) or Raman spectroscopy (Melancon et al., 2005, 2008; Tzeng et al., 2007; Jolivet et al., 2008), but with these methods the whole otolith must be ground to a powder to obtain the average composition. In contrast, neutron diffraction is a method that can allow for non-destructive identification and quantification of CaCO3 polymorphs in an intact otolith; i.e. because of the large penetration depth of neutrons in these materials a whole otolith can be easily sampled. This study uses neutron diffraction analysis to resolve whether sturgeon otoliths contain a non-vaterite fraction and quantify the per cent composition of a non-vaterite fraction if it does exist. Lake sturgeon Acipenser fulvescens Rafinesque 1817 sagittal otoliths (here- after, otoliths; n = 12; Fig. 1) were removed from fish harvested during the annual spear-fishing season on the Lake Winnebago system, Wisconsin, U.S.A. (44∘ 00′ N; 88∘ 30′ W). Harvest of A. fulvescens from the Lake Winnebago system has been actively managed for >100 years and represents one of the only demonstrated sus- tainable sturgeon fisheries in the world (Bruch, 1999). The paddlefish Polyodon spathula (Walbaum 1792) otolith (n = 1) was obtained from the Illinois Department of Natural Resources from a fish collected in the Illinois portion of the Ohio River. While a sample size of one is generally not ideal, limitations on instrument time and sample numbers prevented the examination of more P. spathula otoliths. It was still desirable, however, to characterize this otolith to compare the polymorph composition of A. fulvescens otoliths with that of a closely related species. Also, the novelty of neutron diffraction for characterizing otolith polymorph composition coupled with its sensitivity provided a unique opportunity to create an accurate initial crystallographic characterization of a fish species that had not previously been characterized. Neutrons were chosen because they have a greater penetration depth than X-rays in crystallographic studies. X-rays interact with the electron cloud surrounding each atom and the scattering intensity is proportional to the atomic number, whereas neu- trons interact directly with the nucleus of the atom and the scattering intensity is isotope specific and does not vary periodically. For the elements Ca, C and O, their scattering powers follow the order Ca > C > O for X-rays and O > C > Ca for neutrons. Therefore, neutrons offer a slightly better contrast to determine the carbonate group positions as © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13085 ACIPENSERIDAE OTOLITHS ARE VATERITE AND CALCITE 3 (a) (b) 1 mm Fig. 1. Typical otolith from Acipenser fulvescens: (a) an entire otolith with mm scale and (b) close-up of a vaterite portion of the otolith. compared with that of X-rays. For this study, two neutron diffractometers were used: the nanoscale-ordered materials diffractometer (NOMAD) at the Oak Ridge National Laboratory (ORNL) spallation neutron source [SNS (https://neutrons.ornl.gov/sns/); n = 6 homogenized A. fulvescens otoliths] and the wide-angle neutron diffractome- ter (WAND) at the ORNL’s high flux isotope reactor (https://neutrons.ornl.gov/hfir/; n = 6 whole A. fulvescens otoliths; n = 1 whole P. spathula otolith). The combination of wide detector coverage of NOMAD and high intensity neutron beams available at SNS allowed for measurement of small samples (<100 mg) (Neuefeind et al., 2012), with volumes typically used for X-ray diffraction. The diffraction data were normalized by the scattering from a solid vanadium rod and the background from the empty cap- illary was subtracted. The WAND, in contrast, is a high-intensity, medium-resolution, fixed-wavelength diffractometer. For the 3CaCO polymorphs, NOMAD has sufficient resolution to allow full crystal structure refinements in addition to quantitative phase analysis and the WAND enables quantitative analysis. Because of the high penetration depth of neutrons, the entire volume of the sam- ple was probed in a single diffraction experiment. The preliminary neutron diffrac- tion data collected at NOMAD for shovelnose sturgeon Scaphirhynchus platorynchus (Rafinesque 1820) otoliths (B. C. Chakoumakos, unpubl. data) suggested presence of a calcite fraction, which had not been previously reported in studies of acipenserid otoliths. In developing a protocol for sample preparation and data analysis of otoliths using neutron diffraction, it was considered that the carbonate crystallites in whole otoliths might exhibit a preferred crystallographic orientation, i.e. a singular direc- tion of crystalline growth. In such a case, the radial averaging of data from detectors can result in increased or decreased intensities of particular Bragg peaks. It is well known that preferred orientation can make phase identification and quantitative analy- sis more difficult and reducing or modelling the preferred orientation generally yields more accurate quantitative analysis. Preferred orientation was suspected, but the extent was not known. Another concern was whether the metastable vaterite polymorph could transform to calcite during handling and specimen preparation. Both concerns were tested
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