These pearly white stones are about the size of a pea, and can be found in the fish's skull just below the rear of the brain.
They aren't attached to the skull, but rather float beneath the brain inside the soft, transparent inner ear canals. There are 3 pairs of otoliths in each fish, including 1 large pair the sagittae and 2 small pairs the lapilli and the asteriscii. The largest pair is usually used for determining age. The smaller pairs are about the size of the tip of a pin. However, despite their size, the smallest pair the lapilli is most often used for daily ring ageing. The growth of the otolith is a one-way process.
New otolith material can be and is added to the outside surface through time, but existing material can't be removed. This one-way growth process explains why otoliths can form and retain such delicate structures as daily rings, whereas bone cannot. Otoliths have a very distinct shape, which is characteristic of the species of fish.
That is, different fish species have differently shaped otoliths. The otolith shape is so distinctive that biologists can use otoliths recovered from seal and bird stomachs and droppings to determine the type of fish they ate. Even the size of the otolith can be used to indicate the size of the fish that was eaten. Otoliths of adult fish can generally be removed with nothing more than a sharp fish knife and a pair of forceps or tweezers.
With a little practice, the large pair of otoliths the sagittae can be removed in 15 seconds. Marine fish such as cod and haddock have otoliths which are relatively large and therefore easy to find about 1 cm long in a 30 cm long fish. The largest otolith, which corresponds to the sagitta, is situated in the saccular chamber and a second, slightly smaller second otolith, interpreted as lapillus, occurs in the utriculus of each skeletal labyrinth in all specimens Fig.
A third, rather small otolith, the asteriscus, is present and although its position could not be fully resolved it is considered to be associated with the lagenar chamber. All three otoliths were separated by membrane-like structures Fig. Irregular and unevenly spaced growth rings were found in the otoliths in Amblyraja Fig. Amblyraja radiata exhibits a well-developed sagitta, elongated and thin. The inner face is concave while the outer face is convex.
An extension protrudes into the endolymphatic duct in the 3D reconstruction Fig. This structure, however, was not detected during the dissection but may have been inadvertently sliced away. On the dorsal margin, a prominent bulge is detected in both the reconstruction and the dried otolith Figs. Whether or not this represents a sulcus similar to the one in bony fish cannot be ascertained with certainty due to modification upon air exposure.
The lapillus displays a rounded shape with a single extension protruding caudally Fig. It is flattened except for a bulge on the dorsal margin, which is otherwise slightly concave. The asteriscus is very small in size and elongated in length Fig.
Its morphology is difficult to assess as the structure proved to be very fragile after removal from the inner ear. Further morphological characters are not distinguished in this specimen. Virtual three-dimensional reconstruction of the left skeletal labyrinth and the sagitta and lapillus of Amblyraja radiata and Potamotrygon leopoldi. Red rectangles indicate plane of slicing. The otoliths of Potamotrygon leopoldi display a considerably different morphology compared to Amblyraja radiata.
The sagitta is elongated and rather round with a cranial extension Figs. The sagitta exhibits a very prominent sulcus located almost horizontally over the entire inner face. The lapillus is rounded throughout except for a convex curvature around the posterior margin Figs. In the 3D reconstruction, a slight dorsal extension is visible that probably was damaged during dissection and not found on the dried otolith.
The asteriscus of P. It was not detected in the micro CT scans and its exact position within the skeletal labyrinth was, therefore, difficult to assess. The otoliths of the shark Scyliorhinus canicula differ considerably regarding their morphology.
The sagitta is compact and rounded Fig. There is a prominent bulge on the upper part, followed by a ridge. The edges of the sagitta are rather coarse and a fissure in the lower part of the inner side protrudes ventrally and to the sides.
The lapillus is slightly elongated and ventrally rounded Fig. It is concave and does not show any additional characteristics regarding its morphology. The asteriscus is round and exhibited a gentle curvature throughout the entire surface Fig. All specimens showed considerable differences regarding otolith morphology and shape. Especially, size differences between the lapilli of A. Scyliorhinus canicula otoliths, however, were considerably smaller than in both rays.
Exposure to air showed a stronger impact on the otolith structures of the marine A. Infrared spectroscopy was performed to identify the chemical composition of the otoliths found in P. In general, the spectra contain several regions that are characteristic for various vibrations. C-H stretching vibrations of organic material, e. AR1—3 and SC1—2 are very similar, except that the bands from organic components are stronger in the latter two.
Spectra have been vertically offset for better visibility. We plotted the distribution and composition of otoliths based on our investigations of 89 chondrichthyan individuals combining information from both CT scans and dissections on a phylogenetic tree of vertebrates, with a finer resolution of Chondrichthyes in particular Fig.
Data on the other major vertebrate groups was taken from published sources and Figcombined with the data from our analysis resulting in information for otolith structures and occurrences in 37 different species of cartilaginous fishes, thus providing the most detailed information about such structures in chondrichthyans to date.
The evolutionary relationships between taxa were based on a composite tree drawn from published molecular and morphological data on vertebrates in general [ 51 ], recent data on Acanthodii [ 52 ], recent phylogenetic analyses of basal actinopterygians [ 53 ] and sarcopterygians [ 54 ], and extant chondrichthyans [ 55 , 56 ].
The distribution of three characters morphology, number and composition of otoliths was mapped onto the existing phylogeny to allow a depiction of the range of occurrences of these characters. Otolith structures are widespread among all major chondrichthyan clades and consist of two pairs in most taxa, not exceeding three pairs. Two pairs were found in specimens investigated using CT scans only, while three otoliths were recognized in specimens investigated in situ using dissections.
A shift from calcium phosphate to calcium carbonate material was observed, coinciding with the transformation from agnathans to gnathostomes. Within chondrichthyans, a shift from calcitic otoliths in acanthodians stem group members to apatite otoliths in crown-chondrichthyans occurred.
Phylogeny was composited from overall vertebrate data [ 51 ], acanthodian distribution [ 52 ], basal actinopterygians [ 53 ] and sarcopterygians [ 54 ] and extant chondrichthyan data [ 55 , 56 ].
Otolith morphology and composition for the other major vertebrate groups was taken from literature: Acanthodii [ 13 , 44 , 45 , 47 ], Agnatha [ 8 , 27 , 48 ], Osteichthyes [ 8 , 40 , 41 , 43 , 57 , 58 ].
For the first time, we describe in detail the presence and morphology of endogenous polycrystalline otolith structures within the chondrichthyan skeletal labyrinth and provide an IR spectroscopy analysis of their material composition in representatives of all three major groups within elasmobranchs, including sharks, skates and rays. Our results enable us to propose that some cartilaginous fishes develop three otolith structures in each inner ear similar to what is commonly found in bony fishes, including otoliths of different sizes.
The composition, however, differs considerably, with the integration of phosphate instead of carbonate in the elasmobranchs investigated. Previous studies of otoconial structures within chondrichthyans have focused on their single-crystalline nature and putative carbonate based chemical composition to draw conclusions with regards to the evolution of otoliths in gnathostomes.
A significant result of the present study is that cartilaginous fishes seemingly show a higher variability in the shape as well as the chemical composition of these structures, which may have implications on their evolution throughout vertebrates as discussed below. The elasmobranch specimens here investigated contained otolith structures with a distinct morphology, which differed significantly between A.
Otoliths of A. This may indicate a taxonomic signal in the morphology between different elasmobranch clades. CT scans of additional P. Previous studies assumed that small crystals of different calcium carbonate polymorphs otoconia were embedded upon the sensory macula within the inner ear of both elasmobranchs [ 29 , 30 , 31 , 32 , 37 , 40 , 59 , 60 , 61 ] and holocephalans [ 8 , 22 , 62 ].
Only a single investigation recorded two polycrystalline otolith structures in the elephant fish, Callorhinchus milii , and matched them to the sagitta and asteriscus of bony fish [ 63 ].
Another study reported otoliths in different ontogenetic stages of Leucoraja erinacea but did not elaborate any further on their morphology or composition [ 64 ]. Thus, our results contradict previous findings and raise the question of why large, polycrystalline otoliths have not been reported before with certainty in cartilaginous fishes.
For example, other than the holocephalan study just mentioned, a study focusing on the inner ear morphology in elasmobranchs [ 65 ] clearly showed otoconial masses that we identify as large polycrystalline otoliths here within the otoconial organs but did not mention their morphology or their composition any further. Otolith structures in the ray Raja clavata and the shark Squalus acanthias may have been known for a long time, but either were mistakenly interpreted as a series of singular crystals [ 8 , 24 , 31 , 40 , 60 , 66 ] or only vaguely described without showing the morphology in detail [ 32 , 67 ].
One possible explanation for this is related to the fragile composition of chondrichthyan otoliths when exposed to air. Such decomposition of otoliths into smaller, crystalline units also was observed in the current study; we assume that the binding forces between organic compounds and calcium phosphate crystals are weak compared to those in teleosts.
The observed differences in preservation upon exposure to air between the marine A. A previous study also showed differences in the microchemistry of otolith structures strontium;calcium ratios in three different stingray species, which were linked to the different environments they inhabited [ 68 ].
Additional analyses of the organic compounds binding the apatite crystals therefore are necessary to understand whether the nature of these materials leads to an early fragmentation of otoliths in cartilaginous fishes, which may result in different interpretations from those made previously, but which are beyond the scope of this study.
This could also have implications on the suitability of the morphology of these characters in taxonomic investigations, as the use of these is well-established in bony fishes [e. In the past, chondrichthyan otoconial structures have been reported to be composed of either one of four calcium carbonate polymorphs calcite, vaterite, aragonite or calcium carbonate monohydrate using X-ray powder diffraction analysis [ 8 , 13 , 31 , 72 ].
The present study cannot confirm these findings as all marine A. In addition, our results strongly contradict previous investigations in A. A transformation of minerals from calcium phosphate to calcium carbonate or vice versa within an individual is considered very unlikely as it requires extreme conditions, presumably leading to the destruction of the material, and therefore is rejected [ 13 ]. One earlier study, however, correlated the chemical composition of otoconia in some sharks with changes in ontogeny, showing a gradual replacement but not a transformation of amorphous hydrous calcium phosphate with aragonite material [ 73 ].
A switch from apatite to calcium carbonate has been related to an improved inner ear function as well as an advantage regarding the homeostatic control of different biomineralization processes to be able to regulate otolith and bone deposition independently within the ear [ 8 , 19 , 50 , 74 ]. However, the underlying reasons for an evolutionary shift from phosphate to carbonate otoconial structures between different chondrichthyan taxa, cartilaginous fishes and higher gnathostomes remain ambiguous and are beyond the scope of this work but may be established in future investigations.
Nevertheless, the specimens investigated here do not represent juveniles but rather adults and thus do not contradict our interpretations. The morphology and size of the otoliths within the skeletal labyrinth changed during the evolution of vertebrates. Phosphatic, amorphous single-crystalline bodies characterize living cyclostomes in contrast to polycrystalline otoliths in teleosts and extinct lineages such as acanthodians, as well as the reversion to single-crystalline structures of first aragonite and secondly calcite in sarcopterygians [ 8 , 75 , 76 ].
Establishing the occurrence of polycrystalline otolith structures composed of apatite in chondrichthyans has several implications for the evolution of otoliths in vertebrates. In contrast to earlier assumptions [e. Similarly, proposing the presence of otoconia to be the plesiomorphic state in gnathostomes whereas well-organized otoliths characterize teleosts, may not be as straightforward as previously thought.
In this study, we recovered two to three pairs of otoliths within the inner ears of a broad phylogenetic spectrum of cartilaginous fishes. The difference between two pairs identified in micro CT scans and three pairs from in situ investigations is likely linked to limitations in resolution of these without prior staining of the specific structures, or low mineralization.
In addition to our results, two to three singular otoliths have been reported in acanthodians [ 13 , 14 , 44 , 45 , 46 , 47 ], which have recently been reinterpreted as stem chondrichthyans [e. The otoliths of acanthodians as far as known consist of calcite rather than the apatite we have identified in the elasmobranchs investigated here. In holocephalans, the otoliths have been reported to consist of aragonite [ 22 , 72 ]. The otoliths in the majority of bony fishes consist of calcium carbonate, either in the form of vaterite in all acipenseriforms, most polypteriforms and at least one teleost, or aragonite in a single polypteriform, holosteans, most teleosts, and sarcopterygians with a reversal to calcite in homeothermic tetrapods [ 41 , 72 ].
This short review emphasizes that the chemical composition of otoliths in both chondrichthyans and osteichthyans is not as homogenous as previously thought. The presence of phosphatic otoliths in extant and extinct agnathans [e. However, it previously has been argued that the chemical composition of otoliths correlates with the presence or absence of bony tissues [ 23 ].
Remarkably, vertebrates with no bony or strongly reduced bony tissues such as agnathans and elasmobranchs display phosphatic otoliths, whereas vertebrates with ossified skeletons such as acanthodians and bony fishes have calcitic otoliths. The presence of a largely cartilaginous endoskeleton associated with carbonatic otoliths in acipenseriformes vaterite in Acipenser , vaterite and aragonite in Polypterus does not contradict our interpretation, because the lack of an ossified endoskeleton is considered secondary and the crystals of the otoliths, once deposited, are very resistant to metabolic changes except under extreme stress [ 58 ].
Moreover, the otoliths of Acipenser represent an otoconial mass rather than a solidified polycrystalline otolith as in other bony fishes [ 72 ] consisting of two different parts, a base with a blade-like unit, and an apex resembling an aggregate of fused concretions [ 23 ].
The purposed presence of phosphatic otoliths in Devonian paleonisciform actinopterygians [ 13 , 57 ] also might be related to a reduced endoskeletal ossification but the chemical composition of these otoliths needs to be tested further before final conclusions can be made.
We follow previous hypotheses to assume that the development of endochondral and dermal bones which are apatite-based in fishes may have resulted in the evolution of an independent otolithic system calcium carbonate-based from the skeletal system.
This presumably allowed them to avoid creating an additional system of internal homeostatic balance based on humoral factors associated with bone and mineralization [ 23 ]. It also has been shown that the presence of macromolecules such as glycoproteins and polylactosaminoglycan on or near the maculae influences mineralization of the otoliths [ 77 ]. This further supports the interpretation that the mode of skeletal tissue mineralization influences the chemical composition of otoliths.
One additional advantage of evolving this independent otolithic system, was that changes of the inorganic components and corresponding organic components are assumed to have produced better physical properties of the otolithic apparatus [ 23 ]. Dissection and detailed analyses of the otolith structures in the skeletal labyrinths of the elasmobranchs A.
Differences in the size and shape of otoliths between the two rays and the single shark may indicate a taxonomic signal within elasmobranchs.
Thus, it might be possible to discriminate cartilaginous fishes on different taxonomic levels based on morphological details of their otolith structures. So there is probably a mixture of otoconia degeneration and replacement, with degeneration eventually winning over time.
Another bit of evidence suggesting that otoconia are not replaced is that VEMP's progressively worsen with age -- as VEMP's are mediated by the saccule, one way to explain this would be to postulate that otoconia are progressively lost over time. There are of course many other possible explanations including loss of vestibular neurons. Also supporting the idea that otoconia are never replaced is a NASA study by Parker et al, in which 12 Guinea pigs were centrifuged as high as g to pull off their otoconia.
Some of them were sacrificed acutely and others at 6 months. Exposure to this high acceleration for as little as 20 seconds at G was "sufficient to remove most of the otoconia from the maculae of the saccules and utricles". Parker et al, ; Parker et al, The figure above shows how the righting reflex is absent immediately after high acceleration.
According to this study the righting reflexes sometimes improved at months, although there was no replenishment of otoconia. They state that "There is no adequate evidence from this series of 12 animals that any particular reparative process occurs to explain the return of the righting reflex after exposure".
They were here commenting that the otoconia did NOT return. It would be interesting to see this study replicated. Recall also that guinea pigs and human beings differ very substantially. In another study, when degeneration of otoconia are induced by streptomycin, they are apparently restored within weeks Thalmann et al, Thalmann notes that there seems to be a different situation with these two mechanisms of injury - -with streptomycin injuries recovering, but mechanical ones not.
This is difficult to understand. Our feeling is that almost all of the evidence is for a gradual loss of otoconia through life, and there is little support for the idea that otoconia can regenerate. In aging, the otoconia become roughened, fractured, and hollowed out Ross et al, ; Campos et al, The main route of degeneration is demineralization. According to Walther and Westhoven , the ratio of volume of utricular otoconia between young and elderly was , whereas it was for the saccule.
This is due to normal aging and may explain the progressive loss of VEMP amplitude a measure of the otolith output with age. In Benign Paroxysmal Positional Vertigo BPPV , a common vertigo condition, dizziness is thought to be due to debris, probably otoconial, which has collected within a part of the inner ear. BPPV is much more common in the aged, perhaps due to the degeneration of the otoconia mentioned above.
While otoconia are generally attributed in the literature as being the cause of BPPV, there is no particular reason why otoconial protein matrix, or fragments of other parts of the inner ear might not accumulate, but it would seem likely that such debris would be rapidly disposed, while small stones otoconia , might persist.
Some controversy exists about disposition of debris as some authors e. Zucca et al , feel that stones might dissolve rapidly. In Meniere's disease , it has been suggested by many authors that loose otoconia might block the utricular duct, ductus reuniens, or the endolymphatic duct. Loose giant otoconia such as those that appear in aminoglycoside ototoxicity see next might be even more likely to block the duct. In streptomycin ototoxicity and presumably gentamicin ototoxicity , otoconia not only degenerate but may form giant otoliths.
Ross et al, ; Harada Degenerated otoconia in the aged appear hollowed out -- in ototoxicity they appear dysmorphic. One might then expect more BPPV in ototoxicity, perhaps accompanied by less nystagmus due to the damage to the inner ear.
As we cannot ask a fish how old it is, and that like humans length is not necessarily a good way to distinguish between older fish, otoliths are used instead. Fisheries scientists routinely estimate fish ages by counting otolith growth rings.
Researchers also use otoliths to reconstruct fish life histories. As the water around a fish is constantly changing either through it flowing or the fish moving , the trace chemistry of an otolith ring will also change. Basically, as an otolith ring is formed, some trace salts from the environment also get incorporated into the ring.
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