Structural variation in the inner ears of four deep‐sea elopomorph fishes

Abstract

Deep-sea fishes have evolved in dark or dimly lit environments devoid of the visual cues available to shallow-water species. Because of the limited opportunity for visual scene analysis by deep-sea fishes, it is reasonable to hypothesize that the inner ears of at least some such species may have evolved structural adaptations to enhance hearing capabilities in lieu of vision. As an initial test of this hypothesis, scanning electron microscopy was used to examine the structure of the inner ears of four deep-sea elopomorph species inhabiting different depths: Synaphobranchus kaupii, Synaphobranchus bathybius, Polyacanthonotus challengeri, and Halosauropsis macrochir. The shape of the sensory epithelia and hair cell ciliary bundle orientation of the saccule, lagena, and utricle, the three otolithic organs associated with audition and vestibular function, are described. The saccules of all four species have a common, alternating ciliary bundle orientation pattern. In contrast, the lagena exhibits more interspecific diversity in shape and ciliary bundle orientation, suggesting that it has special adaptations in these species. The macula neglecta, a sensory epithelium of unknown function, is present in all four species.

Inner Ear Morphology in the Atlantic Molly Poecilia mexicana—First Detailed Microanatomical Study of the Inner Ear of a Cyprinodontiform Species

“…This relative (microscopic) motion between otolith and sensory epithelium is either caused by swimming (linear or vertical acceleration) or sound stimulation in terms of particle motion [21], [36], [37]. Like P. mexicana and X. eiseni , there are several species that reveal maculae sacculi and/or maculae lagenae partly not covered by the respective otolith, e.g., yellow perch, Perca flavescens [3] (Percidae), lake whitefish, Coregonus clupeaformis [19] (Salmonidae), as well as some deep-sea fishes [5], [6]. According to the ‘quadrupole model’, uncovered hair cells should work as lateral quadrupole sensors, while hair cells that are covered by the otolith may act as dipole sensors [38].…”

“…According to their position in the inner ear, three different otolith types can be distinguished, namely the otolith of the utricle (lapillus), saccule (sagitta), and lagena (asteriscus). Otoliths can either cover the entire macula or only a part of it [3], [5], [6], [19]; in the latter case, the remaining macula area is covered by the otolithic membrane only. Still, the interrelationships between otolith morphology, and features like otolithic membrane structure, or the structure of the respective sensory epithelium are not yet fully understood [20], [21].…”

Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology

“…In addition, Amia calva exhibits a striola-like region that resembles that of the utricular maculae (Popper and Northcutt, 1983), and Lepisosteus osseus displays three instead of two orientation groups (Mathiesen and Popper, 1987). Three groups are also found in some members of the Elopomorpha (Anguilla anguilla; Figure 10D; Mathiesen, 1984), especially in some deepsea elopomorphs (Buran et al, 2005) or the chaetodontid Chaetodon miliaris (Popper, 1977); but in these teleosts the third orientation group is restricted to a very narrow band at the posterior margin of the macula lagenae (Mathiesen and Popper, 1987).…”

Are accessory hearing structures linked to inner ear morphology? Insights from 3D orientation patterns of ciliary bundles in three cichlid species

“…When considering the natural 3D curvature of the maculae, however, orientation patterns of ciliary bundles on the macula lagenae in E. maculatus did show a more complex pattern, as the ciliary bundles on the anterior-most portion of the macula lagenae formed additional orientation groups. Such a 3D arrangement of ciliary bundles was previously found in the anterior region (ostium) of the macula sacculi of silver perch [23], the ostium of the macula sacculi of the non-teleost bowfin Amia calva (Neopterygii, Amiidae) [40], and in the macula lagenae of the deep-sea dwelling elopomorph Polyacanthonotus challenger [41]. The wider range of directions of ciliary bundles based on the 3D curvature of the respective macula ought to translate into a wider range of directional stimuli being detectible, and hence ought to play a crucial role in sound source localization.…”