Trace element–protein interactions in endolymph from the inner ear of fish: implications for environmental reconstructions using fish otolith chemistry

Abstract

Otoliths, the biomineralised hearing "ear stones" from the inner ear of fish, grow throughout the lifespan of an individual, with deposition of alternating calciferous and proteinaceous bands occurring daily. Trace element : calcium ratios within daily increments measured by laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS) are often used in fisheries science to reconstruct environmental histories. There is, however, considerable uncertainty as to which elements are interacting with either the proteinaceous or calciferous zones of the otolith, and thus their utility as indicators of environmental change. To answer this, we used size exclusion chromatography-inductively coupled plasma-mass spectrometry (SEC-ICP-MS) of endolymph, the otolith growth medium, to determine the binding interactions for a range of elements. In addition, we used solution ICP-MS to quantify element concentrations in paired otolith and endolymph samples and determined relative enrichment factors for each. We found 12 elements that are present only in the proteinaceous fraction, 6 that are present only in the salt fraction, and 4 that are present in both. These findings have important implications for the reconstruction of environmental histories based on changes in otolith elemental composition: (1) elements occurring only in the salt fraction are most likely to reflect changes in the physico-chemical environment experienced during life; (2) elements occurring only in the proteinaceous fraction are more likely to reflect physiological rather than environmental events; and (3) elements occurring in both the salt and proteinaceous fractions are likely to be informative about both endogenous and exogenous processes, potentially reducing their utility in environmental reconstructions.

Otolith chemistry does not just reflect environmental conditions: A meta‐analytic evaluation

“…This effect parallels observations of aqueous Ba generally increasing towards fresher waters (Coffey et al., ). Furthermore, Ba has a larger ionic radius than Ca and is preferentially bound to aragonite relative to Sr at time of accretion, with the rate of elemental substitutions for Ca in the otolith matrix dependent on ambient concentration and uptake kinetics (Loewen et al., ; Thomas et al., ). Thus, increases in water Ba are reflected in otolith chemistry, reinforcing the reputation of this element in environmental reconstructions, which partially justifies the lack of importance of analysed covariates in the water–otolith meta‐analysis.…”

“…In tandem, more comprehensive in situ experiments as well as further evaluations of intrinsic factors on otolith chemistry should be pursued to disentangle the limits and conditions where otolith chemistry can effectively and reliably reflect environmental conditions. These experiments should be extended to consider changes to ion–protein interactions, given that these are likely the common mechanism via which physiological processes modify element availability and incorporation into the otolith (Sturrock et al., ), namely to evaluate how plasma protein concentrations determine ion availability in the endolymph and subsequent otolith chemistry (Grønkjær, ; Thomas et al., ). There is also growing evidence of the role of a suite of intrinsic factors influential on otolith elemental incorporation (e.g., growth rate, ontogeny, maturation/reproduction, condition, sex or genetics and population specific responses to name but a few: Chang & Geffen, ; Clarke et al., ; Izzo et al., ; Secor & Rooker, ; Stanley et al., ; Sturrock et al., ; Turner & Limburg, ), and this requires further investigation.…”

“…Otoliths biomineralize material on a daily timescale forming distinguishable time‐resolved growth increments that incorporate elements into the precipitating surface of the structure. Elements may directly substitute for Ca in the otolith CaCO 3 and/or form metal–protein binding complexes, remaining stable within the metabolically inert otolith crystalline structure (Campana, ; Doubleday, Harris, Izzo, & Gillanders, ; Izzo, Doubleday, & Gillanders, ; Thomas, Ganio, Roberts, & Swearer, ). Otolith elements are primarily sourced from the surrounding environment, with water chemical composition and its physical–chemical properties (e.g., salinity and temperature) underpinning variations in otolith chemistry (Elsdon & Gillanders, ; Miller, ; Reis‐Santos, Tanner, Elsdon, Cabral, & Gillanders, ).…”

Spatial and temporal variation in otolith chemistry and its relationship with water chemistry: Stock discrimination of Sperata aor

“…The rate of substitution of these elements could be regulated by the ambient water and the concentrations within the endolymph (Thomas, Ganio, Roberts, & Swearer, 2017). The rate of substitution of these elements could be regulated by the ambient water and the concentrations within the endolymph (Thomas, Ganio, Roberts, & Swearer, 2017).…”

“…Sr and Ba show considerable levels of enrichment in the otolith; thereby, these elements can be appropriately used to discriminate fish stocks (Thomas et al, 2017). These elements in the otoliths show low enrichment; therefore, the utility of these elements in stock discrimination is limited (Thomas et al, 2017). These elements in the otoliths show low enrichment; therefore, the utility of these elements in stock discrimination is limited (Thomas et al, 2017).…”