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outside the range of the qui note. These sex differences reflect the function of the qui note in attracting females to the male for mating (Narins and Capranica, 1976).
Tadpoles Hear Through Extratympanic Routes
Tadpole metamorphosis features remarkable changes in body morphology: first the hind limbs then the fore limbs emerge, the tail is absorbed into the body, and the small tadpole oral disk transforms into the large frog mouth (see In species such as the bullfrog where an aquatic tadpole transforms into a terrestrial frog, the metamorphic transition impacts how sounds are processed because of the different acoustic properties of underwater and terrestrial environments (Popper and Hawkins, 2018). To prepare for the new terrestrial soundscape, the ability to hear airborne sounds should emerge prior to the final emergence to land. Hence, we expect considerable maturation of hearing capabilities before metamorphosis is complete.
Ear development in terrestrial frogs follows an inside-out or medial-to-lateral trajectory (Simmons, 2019; Womack et al., 2016): The inner ear organs develop before the middle ear, and the middle ear develops before the external tympanum (Figure 3).
Development of the inner ear organs begins with the formation and differentiation of the saccule, followed by that of the amphibian and basilar papillae (Simmons and Alexander, 2014). These three organs all have the same shape in tadpoles (Figure 4) as they do in adults, but they are smaller and contain fewer hair cells. Developmental changes in hair cell numbers and in numbers of eighth nerve fibers innervating these hair cells have been quantified for the saccule (Simmons and Alexander, 2014), but little is known about these events in the two auditory papillae.
The in-outside developmental trajectory from the inner ear to the external tympanum is illustrated in Figure 3. The oval window is present in the otic capsule early in tadpole life, right after hatching. Around the time of emergence of the hind limbs, the operculum becomes visible at one end of the oval window (Figure 3D; Hetherington, 1987; Horowitz et al., 2001). Later, around the time that the tadpole develops its fore limbs, opercularis muscle fibers can be seen inserting into the operculum (Hetherington, 1987). Thus, the operculum transmission pathway is functional
before metamorphosis is complete. Although tadpoles have lungs, the Eustachian tubes and the large mouth cavity do not appear until after the final transition to land.
The tympanic pathway, in contrast, is not fully developed until sometime after the completion of metamorphosis. In bullfrog tadpoles, the columella footplate begins to differentiate around the time of fore limb development (Figures 3C and 6). The columella is visible at the end of metamorphosis (Figure 3B). But the external tympanum (Figure 3A) does not appear until sometime after the froglet has moved to land. The time course of tympanum development varies between species, from 24 to 48 hours after the end of metamorphosis in bullfrogs (Boatright- Horowitz and Simmons, 1995) to 60 days later in spring peepers Pseudacris crucifer (Hetherington, 1987) and even 15 weeks later in the giant toad Rhinella horribilis (Womack et al., 2018). These delays in the emergence of the tympanum suggest that froglets in their terrestrial environments have poor sensitivity to airborne sounds (Womack et al., 2016). But we understand little about the role of sounds in the lives of froglets, so the biological
  Figure 6. Left: horizontal section through the otic capsule of a bullfrog tadpole immediately before the completion of metamorphosis. The columella has not reached its mature length, the extracolumella has not yet begun to form, and the external tympanum is absent (see Figure 3B). Shades of blue indicate cartilage. cf, Columella footplate; ow, oval window; op, operculum; s, saccule. Medial is to the right and lateral is to the left. Scale bar, 500 μm. Images used with permission, copyright © 2020 A. M. Simmons, all rights reserved. Right: bullfrog tadpole near the completion of metamorphosis. Hind limbs, fore limbs, and tail are present, but no external tympanum is visible. Photo courtesy of Nature Picture Library/Alamy stock photo, used with permission.
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