Comparative and developmental patterns of amphibious auditory function in salamanders

Abstract

Early amphibious tetrapods may have detected aquatic sound pressure using sound-induced lung vibrations, but their lack of tympanic middle ears would have restricted aerial sensitivity. Sharing these characteristics, salamanders could be models for the carryover of auditory function across an aquatic-terrestrial boundary without tympanic middle ears. We measured amphibious auditory evoked potential audiograms in five phylogenetically and ecologically distinct salamanders (Amphiuma means, Notophthalmus viridescens, Ambystoma talpoideum, Eurycea spp., and Plethodon glutinosus) and tested whether metamorphosis and terrestrial niche were linked to aerial sensitivity. Threshold differences between media varied between species. A. means' relative aerial sensitivity was greatest at 100 Hz and decreased with increasing frequency. In contrast, all other salamanders retained greater sensitivity up to 500 Hz, and in A. talpoideum and Eurycea, relative sensitivity at 500 Hz was higher than at 100 Hz. Aerial thresholds of terrestrial P. glutinosus above 200 Hz were similar to A. talpoideum and Eurycea, but lower than N. viridescens and A. means. Metamorphosis did not affect aerial sensitivity in N. viridescens or A. talpoideum. These results fail to support a hypothesis of terrestrial hearing specialization across ontogeny or phylogeny. We discuss methodological limitations to our amphibious comparisons and factors affecting variation in amphibious performance.

Gene, cell, and organ multiplication drives inner ear evolution

“…5). Salamanders lack a tympanic ear and show limited sensitivity to sound (Zeyl and Johnston, 2016) but have a basilar papilla with separate sensory projection within the CNS though they lack morphologically-distinct auditory nuclei (Herrick, 1948; Nieuwenhuys et al, 1998; Will and Fritzsch, 1988). Similar segregated projections in the absence of nuclei were found in the visual system (Fritzsch, 1980) and might indicate a more general evolutionary principle, segregated neuropils appear before segregated nuclei (Herrick, 1948).…”

Underwater sound production varies within not between species in sympatric newts

“…Acoustic sense abilities are unknown in the examined taxa. Hearing ability in the North-American newt genus Notophthalmus is less sensitive than in other salamanders (Zeyl & Johnston, 2016). Generally, salamanders and newts lack a tympanum and middle ear, but they may detect sounds through extratympanic pathways, such as an air-filled mouth cavity (Bulog & Schlegel, 2000) or air volumes in their lungs (Christensen et al, 2015).…”

“…Although caudate amphibians lack an ear opening and middle ear, this poses no limitation for their high frequency hearing underwater. Their ability to detect sounds covers wide frequency ranges (Bulog & Schlegel, 2000), whereas others reported declining underwater hearing abilities towards high frequencies (Crovo, Zeyl & Johnston, 2016; Zeyl & Johnston, 2016). Despite mixed information about the extent of underwater hearing in salamanders, their conspecific sound detection ability may depend not only on hearing capabilities but also on acoustic divergence between individuals, sexes, or species occupying the same habitat, similar to anurans (Littlejohn, 1977; Gerhardt & Schwartz, 1995; Leininger & Kelley, 2015; but see Amézquita et al, 2011).…”