An official website of the United States government
Ocean acidification, the ongoing decline of surface ocean pH and [CO$${}_{3}^{2-}$$] due to absorption of surplus atmospheric CO 2 , has far-reaching consequences for marine biota, especially calcifiers. Among these are teleost fishes, which internally calcify otoliths, critical elements of the inner ear and vestibular system. There is evidence in the literature that ocean acidification increases otolith size and alters shape, perhaps impacting otic mechanics and thus sensory perception. Here, larval Clark’s anemonefish, Amphiprion clarkii (Bennett, 1830), were reared in various seawater pCO 2 /pH treatments analogous to future ocean scenarios. At the onset of metamorphosis, all otoliths were removed from each individual fish and analyzed for treatment effects on morphometrics including area, perimeter, and circularity; scanning electron microscopy was used to screen for evidence of treatment effects on lateral development, surface roughness, and vaterite replacement. The results corroborate those of other experiments with other taxa that observed otolith growth with elevated pCO 2 , and provide evidence that lateral development and surface roughness increased as well. Both sagittae exhibited increasing area, perimeter, lateral development, and roughness; left lapilli exhibited increasing area and perimeter while right lapilli exhibited increasing lateral development and roughness; and left asterisci exhibited increasing perimeter, roughness, and ellipticity with increasing pCO 2 . Right lapilli and left asterisci were only impacted by the most extreme pCO 2 treatment, suggesting they are resilient to any conditions short of aragonite undersaturation, while all other impacted otoliths responded to lower concentrations. Finally, fish settlement competency at 10 dph was dramatically reduced, and fish standard length marginally reduced with increasing pCO 2 . Increasing abnormality and asymmetry of otoliths may impact inner ear function by altering otolith-maculae interactions.
more »
« less
First paleoproteome study of fossil fish otoliths and the pristine preservation of the biomineral crystal host
Abstract Otoliths are calcium carbonate components of the stato-acoustical organ responsible for hearing and maintenance of the body balance in teleost fish. During their formation, control over, e.g., morphology and carbonate polymorph is influenced by complex insoluble collagen-like protein and soluble non-collagenous protein assemblages; many of these proteins are incorporated into their aragonite crystal structure. However, in the fossil record these proteins are considered lost through diagenetic processes, hampering studies of past biomineralization mechanisms. Here we report the presence of 11 fish-specific proteins (and several isoforms) in Miocene (ca. 14.8–14.6 Ma) phycid hake otoliths. These fossil otoliths were preserved in water-impermeable clays and exhibit microscopic and crystallographic features indistinguishable from modern representatives, consistent with an exceptionally pristine state of preservation. Indeed, these fossil otoliths retain ca. 10% of the proteins sequenced from modern counterparts, including proteins specific to inner ear development, such as otolin-1-like proteins involved in the arrangement of the otoliths into the sensory epithelium and otogelin/otogelin-like proteins that are located in the acellular membranes of the inner ear in modern fish. The specificity of these proteins excludes the possibility of external contamination. Identification of a fraction of identical proteins in modern and fossil phycid hake otoliths implies a highly conserved inner ear biomineralization process through time.
more »
« less
- Award ID(s):
- 1855381
- PAR ID:
- 10467936
- Publisher / Repository:
- Springer Nature
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Typical analyses of otolith microchemistry use calcium, a major constituent, as an internal standard, setting its value as a constant and ignoring any potential variations. In fact, patterns do occur in otolith Ca deposition, as can be observed either by repeating the analysis, by creating two-dimensional maps of Ca, or both. Here we present evidence of Ca variations in fish otoliths from analyses using synchrotron-based scanning X-ray fluorescence microscopy, electron microprobe analysis, and laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). 2-D maps of otoliths created with LA-ICP-MS indicate that Ca is elevated where especially Zn and P are low, and vice versa, suggesting that spatial variations in protein deposition may affect concentrations of Ca. We encourage others to examine Ca concentrations in their biomineralized samples to check for variations, using LA-ICP-MS and other methods.more » « less
-
Otolith chemistry has gained increasing attention as a tool for analyzing various aspects of fish biology, such as stock dynamics, migration patterns, hypoxia and pollution exposure, and connectivity between habitats. While these studies often assume otolith elemental concentrations reflect environmental conditions, physiological processes are increasingly recognized as a modulating and/or controlling factor. In particular, biomineralization—the complex, enzyme-regulated construction of CaCO3 crystals scaffolded by proteins—is believed to play a critical role in governing otolith chemical patterns. This review aims to summarize the knowledge on otolith composition and biophysical drivers of biomineralization, present hypotheses on how biomineralization should affect element incorporation, and test the validity thereof with selected case studies. Tracers of environmental history are assumed to be dominated by elements that substitute for Ca during crystal growth or that occur randomly trapped within the crystal lattice. Strontium (Sr) and barium (Ba) largely comply with the biomineralization-based hypotheses that otolith element patterns reflect environmental concentrations, without additional effects of salinity, but can be influenced by physiological processes, typically exhibiting decreasing incorporation with increasing growth. Conversely, tracers of physiology are assumed to be elements under physiological control and primarily occur protein-bound in the otolith’s organic matrix. Physiological tracers are hypothesized to reflect feeding rate and/or growth, decrease with fish age, and exhibit minimal influence of environmental concentration. The candidate elements phosphorus (P), copper (Cu) and zinc (Zn) confirm these hypotheses. Magnesium (Mg) is believed to be randomly trapped in the crystal structure and hence a candidate for environmental reconstruction, but the response to all examined drivers suggest Mg to be coupled to growth. Manganese (Mn) substitutes for Ca, but is also a co-factor in matrix proteins, and therefore exhibits otolith patterns reflecting both environmental (concentration and salinity) and physiological (ontogeny and growth) histories. A consistent temperature response was not evident across studies for either environmental or physiological tracers, presumably attributable to variable relationships between temperature and fish behavior and physiology (e.g., feeding rate, reproduction). Biomineralization thus has a controlling effect on otolith element concentrations for elements that are linked with somatic growth, but not for elements that substitute for Ca in the crystal lattice. Interpretation of the ecological significance of patterns from field samples therefore needs to consider the impact of the underlying biomineralization processes of the element in question as well as physiological processes regulating the availability of ions for inclusion in the growing crystal lattice. Such understanding will enhance the utility of this technique to address fisheries management questions.more » « less
-
Understanding how humans have altered coral reef food webs remains challenging due to the absence of prehistoric baselines. Here, we use fish remains preserved in fossil and archaeological deposits from Panamá and the Dominican Republic to explore how Caribbean reef fish mortality patterns have changed over millennia. By quantifying accumulation rates of shark dermal denticles (scales) and bony fish otoliths (ear stones) in reef sediments, we assess relative fish abundance, while otolith size serves as a proxy for body size at death. Comparisons of these death assemblages suggest a 75% decline in shark-derived material and a 22% reduction in the sizes of human-targeted fishes—consistent with historical exploitation. This evidence of decline in large-bodied, higher trophic level fish remains coincided with a doubling in prey fish otolith accumulation and a 17% increase in their reconstructed body sizes. These patterns in time-averaged death assemblages align with effects of release from predation, documenting an often assumed (but rarely shown) cascading effect. In contrast, otoliths of predator-sheltered cryptobenthic fishes showed no change in either accumulation or size, suggesting that ‘‘bottom–up”environmental factors were not responsible for the observed changes. Together, these data indicate that pre-exploitation predator communities strongly controlled exposed prey fishes, but this “top–down” effect diminishes rapidly toward the food chain base, especially in predator-resistant groups. Understanding trophic cascades on Caribbean reefs requires studying systems before predator depletion.more » « less
-
The inner ear is essential for maintaining balance and hearing predator and prey in the environment. Each inner ear contains three CaCO3 otolith polycrystals, which are calcified within an alkaline, K+-rich endolymph secreted by the surrounding epithelium. However, the underlying cellular mechanisms are poorly understood, especially in marine fish. Here, we investigated the presence and cellular localization of several ion-transporting proteins within the saccular epithelium of the Pacific Chub Mackerel (Scomber japonicus). Western blotting revealed the presence of Na+/K+-ATPase (NKA), carbonic anhydrase (CA), Na+-K+-2Cl--co-transporter (NKCC), vacuolar-type H+-ATPase (VHA), plasma membrane Ca2+ ATPase (PMCA), and soluble adenylyl cyclase (sAC). Immunohistochemistry analysis identified two distinct ionocytes types in the saccular epithelium: Type-I ionocytes were mitochondrion-rich and abundantly expressed NKA and NKCC in their basolateral membrane, indicating a role in secreting K+ into the endolymph. On the other hand, Type-II ionocytes were enriched in cytoplasmic CA and VHA, suggesting they help transport HCO3- into the endolymph and remove H+. In addition, both types of ionocytes expressed cytoplasmic PMCA, which is likely involved in Ca2+ transport and homeostasis, as well as sAC, an evolutionary conserved acid-base sensing enzyme that regulates epithelial ion transport. Furthermore, CA, VHA, and sAC were also expressed within the capillaries that supply blood to the meshwork area, suggesting additional mechanisms that contribute to otolith calcification. This information improves our knowledge about the cellular mechanisms responsible for endolymph ion regulation and otolith formation, and can help understand responses to environmental stressors such as ocean acidification.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41598-023-30537-8
