Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths

Abstract

Otoliths in bony fishes play an important role in the senses of balance and hearing. Otolith mass and shape are, among others, likely to be decisive factors influencing otolith motion and thus ear functioning. Yet our knowledge of how exactly these factors influence otolith motion is incomplete. In addition, experimental studies directly investigating the function of otoliths in the inner ear are scarce and yield partly conflicting results. Herein, we discuss questions and hypotheses on how otolith mass and shape, and the relationship between the sensory epithelium and overlying otolith, influence otolith motion. We discuss (i) the state‐of‐the‐art knowledge regarding otolith function, (ii) gaps in knowledge that remain to be filled, and (iii) future approaches that may improve our understanding of the role of otoliths in ear functioning. We further link these functional questions to the evolution of solid teleost otoliths instead of numerous tiny otoconia as found in most other vertebrates. Until now, the selective forces and/or constraints driving the evolution of solid calcareous otoliths and their diversity in shape in teleosts are largely unknown. Based on a data set on the structure of otoliths and otoconia in more than 160 species covering the main vertebrate groups, we present a hypothetical framework for teleost otolith evolution. We suggest that the advent of solid otoliths may have initially been a selectively neutral ‘by‐product’ of other key innovations during teleost evolution. The teleost‐specific genome duplication event may have paved the way for diversification in otolith shape. Otolith shapes may have evolved along with the considerable diversity of, and improvements in, auditory abilities in teleost fishes. However, phenotypic plasticity may also play an important role in the creation of different otolith types, and different portions of the otolith may show different degrees of phenotypic plasticity. Future studies should thus adopt a phylogenetic perspective and apply comparative and methodologically integrative approaches, including fossil otoliths, when investigating otoconia/otolith evolution and their function in the inner ear.

Lagenar potentials of the vocal plainfin midshipman fish, Porichthys notatus

“…Although the auditory end organs of most teleost fishes primarily serve as biological accelerometers to detect particle motion (de Vries 1950; Hawkins 1993; Sisneros and Rogers 2016; Schulz-Mirbach et al 2018), some fish have evolved adaptations that allow them to detect pressure. For instance, Otophysan fishes (e.g., goldfish, zebrafish, catfishes, and relatives) possess specialized structures or skeletal adaptations (e.g., the Weberian ossicles in goldfish) that allow for the transfer of acoustic energy from the swim bladder to the inner ear.…”

“…Like most teleost fishes, midshipman have an inner ear which consists of three semicircular canals that encode angular momentum (vestibular function) and three otolithic end organs (saccule, lagena, and utricle) that may serve an auditory and/or vestibular (positional) function, however, to what extent each end organ contributes to audition is unknown and likely varies between taxa (Platt and Popper 1981; Popper and Fay 1993; Schulz-Mirbach et al 2018). The otolithic end organs essentially act as biological accelerometers that are sensitive to acoustic particle motion (de Vries 1950; Fay 1984).…”

“…Of the three end organs, the saccule is often the largest and most implicated in terms of hearing for most teleost fishes (Popper and Fay 1993). While a number of studies have characterized the response properties of the teleost saccule and its auditory afferents, very few studies have examined the auditory response properties and acoustic function of the teleost lagena and utricle (Schulz-Mirbach et al 2018). A small number of studies suggest that both the lagena and utricle are capable of coding acoustic particle motion (Lu et al 2003, 2004; Meyer et al 2004, 2010; Maruska and Mensinger 2015), but the possible acoustic functions of the lagena and utricle are still not yet well understood.…”

Otoliths of sub‐adult Lake Sturgeon Acipenser fulvescens contain aragonite and vaterite calcium carbonate polymorphs

“…Hitherto, the crystallisation of aragonite otoliths was not thought to have evolved until the separation of teleosts from other Actinoperygian fishes ( e.g ., sturgeon, paddlefish, gar; Carlström ; Fermin et al ., ; Gauldie, , Pracheil et al ., in press). Although small calcite and aragonite inclusions have indeed been observed in the otoliths of other acipenserids, they were believed to be an artifact of preservation or a transformation to more stable crystalline forms post‐dissection rather than true observations of non‐vaterite otoliths (Carlström, ; Lychakov, ; Schulz‐Mirback et al ., ). Mechanical and thermodynamic testing of vaterite transformation confirmed, however, that although the vaterite polymorph found in Lake Sturgeon otoliths is metastable, it is indeed resistant to transformation to more stable polymorphs under routine methods (Pracheil et al ., ).…”

An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes

“…The ear consists of three semi‐circular canals and associated sensory regions (ampullae) that are primarily involved in detection of angular acceleration and three otolith organs (saccule, lagena, utricle) that are involved in hearing and positional senses (Popper et al, ). There is very substantial variation in the morphology of the ears of fishes and particularly in the regions associated with hearing (Ladich & Schulz‐Mirbach, ; Retzius, ; Schulz‐Mirbach et al, ; Schulz‐Mirbach & Ladich, ), leading to the suggestion that there is very substantial diversity in hearing mechanisms (and potentially capabilities) in different species (Popper et al, ).…”