Sensory surface of the saccule and lagena in the ears of ostariophysan fishes

Abstract

The inner ears of a few fishes in the teleost superorder Ostariophysi are structurally unlike those of most other teleosts. Scanning electron microscopy was used to determine if other ostariophysans share these unusual features. Examined were the families Cyprinidae, Characidae, and Gymnotidae (all of the series Otophysi), and Chanidae (of the sister series Anotophysi), representing the four major ostariophysan lineages, the auditory organs of which have not yet been well described. Among the Otophysi, the saccular and lagenar otolith organs are similar to those reported for other ostariophysans. The lagena is generally the larger of the two organs. The saccular sensory epithelium (macula) contains long ciliary bundles on the sensory hair cells in the caudal region, and short bundles in the rostral region. The saccule and the lagena each have hair cells organized into two groups having opposing directional orientations. In contrast, Chanos, the anotophysan, has a saccular otolith larger than the lagenar otolith, and ciliary bundles that are more uniform in size over most of its saccular macula. Most strikingly, its saccular macula has hair cells organized into groups oriented in four directions instead of two, in a pattern very similar to that in many nonostariophysan teleosts. We suggest that the bi-directional pattern seen consistently in the Otophysi is a derived development related to particular auditory capabilities of these species.

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

“…The second hypothesis assumes that the ancestral teleost condition is the pattern including vertical and horizontal groups and that horizontal groups were lost twice, in otophysans and mormyrids. If the second hypothesis applies-which is the more parsimonious one-the vertical pattern in otophysans and mormyrids may have convergently evolved due to similar selection pressures (Popper and Platt, 1983). The vertical pattern is the constant element in each of the five different orientation patterns on the macula sacculi in teleosts (Popper, 1981), and the vertical pattern is also found in Chondrichthyes, lungfishes, and non-teleost actinopterygians (see above; Popper and Fay, 1977;1993).…”

“…In these taxa, the semicircular canals run around the large saccule rather than being located dorsally to it. Most otophysans are characterized by having a lagena as large as or larger than the elongate saccule (Figure 2A; Popper and Platt, 1983). In ariid catfishes, however, the utricle is distinctly larger than both saccule and lagena (Popper and Tavolga, 1981).…”

“…Tetrapods have only two "vertical" groups on the macula sacculi and this may also hold true for cartilaginous fishes, nonteleost actinopterygians and lungfishes: the horizontal groups in these fishes are classified to be no "true" horizontal groups because originally vertically oriented ciliary bundles simply follow the curvature of the closest macula margin, gradually leading to an increased horizontal-like orientation (Figure 8; Platt, 1983, Popper andFay, 1993). Two alternative hypotheses have been discussed (Popper and Platt, 1983). First, the vertical pattern is an ancestral pattern that was retained in otophysans and mormyrids, whereas in the remaining teleosts true horizontal groups evolved at least seven times independently.…”

“…Some teleost taxa with accessory auditory structures such as mormyrids (Popper, 1981), otophysans (e.g., Popper and Platt, 1983), and the cichlid E. maculatus (Schulz-Mirbach et al, 2014) possess a large macula lagenae that may be even larger than the maculae sacculi (Popper et al, 2003). In addition, the maculae lagenae of otophysans tend to be oriented more along the antero-posterior axis than stretching along a dorso-ventral or posteroventral to anterodorsal axis (compare Figures 10A,C,G with Figures 10E,H).…”

Infrasound initiates directional fast-start escape responses in juvenile roachRutilus rutilus

“…While the sacculus in the ostariophysi appears to be dedicated to encoding phases of sound pressure, the direction of initial acceleration may be encoded by the utricle and the lagena (see review by Popper and Edds-Walton, 1995). In both these otolith organs the hair cells are distributed with sensory axes at a variety of angles across the sensory epithelium (Popper and Platt, 1983;Platt, 1993). Casagrand et al (1999) have shown that both sound pressure and acceleration cause excitatory postsynaptic potentials in Mauthner neurons and homologous cells, but sound pressure was a much more efficient stimulator than acceleration.…”