How minute sooglossid frogs hear without a middle ear

Abstract

Acoustic communication is widespread in animals. According to the sensory drive hypothesis [Endler JA (1993) Philos Trans R Soc Lond B Biol Sci 340(1292): [215][216][217][218][219][220][221][222][223][224][225], communication signals and perceptual systems have coevolved. A clear illustration of this is the evolution of the tetrapod middle ear, adapted to life on land. Here we report the discovery of a bone conduction-mediated stimulation of the ear by wave propagation in Sechellophryne gardineri, one of the world's smallest terrestrial tetrapods, which lacks a middle ear yet produces acoustic signals. Based on X-ray synchrotron holotomography, we measured the biomechanical properties of the otic tissues and modeled the acoustic propagation. Our models show how bone conduction enhanced by the resonating role of the mouth allows these seemingly deaf frogs to communicate effectively without a middle ear.earless frog | audition | extra-tympanic pathways | X-ray imaging T he middle ear evolved multiple times independently during the evolution of terrestrial life (1). Indeed, a tympanic middle ear is an adaptation to life on land (2, 3) and compensates for the mismatch in acoustic impedance between air and tissue. Without it, 99.9% of sound energy is reflected by the body wall (4, 5). Sechellophryne gardineri is one of the world's smallest terrestrial tetrapods (6). These sooglossid frogs have a Gondwanan origin and evolved in isolation on the Seychelles Archipelago over the last [47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64][65]8). They lack a middle ear yet produce acoustic signals (9, 10). In fact, similar to many species of frogs lacking the tympanic middle ear, they are still capable of hearing in air. Nevertheless, the mechanisms for sound transfer to the inner ear are far less clear. Some extratympanic pathways (11) such as the lungs (12), the opercular system (13), and bone conduction (14) have been proposed but remain to be tested experimentally (11). X-ray synchrotron holotomography of a female S. gardineri reveals that the pulmonary system is poorly developed and cannot contribute significantly to a lung-based sound transmission pathway. We used finite-difference simulations to investigate possible pathways through the head itself. These simulations highlighted the role of the mouth. Finite-element simulations further showed that the oral cavity of the animals resonates at the dominant frequency of the advertisement call of the species. In addition, synchrotron holotomography performed on seven different species showed that earless frogs are specialized for sound transmission between the oral cavity and the ears in two ways: (i) by minimizing the tissue thickness between the mouth and the inner ear and (ii) by minimizing the number of layers of tissue. The combination of these extratympanic pathways allows the frog to perceive sound efficiently.

A cost-effectiveness analysis of a 10-valent pneumococcal conjugate vaccine in children in six Latin American countries

“…Demographic estimates for 2008 grouped by age and gender were used for each country to convert rates into absolute numbers as required by the model [17-21]. In the case of Peru and Argentina, demographic estimates used corresponded to 2007 and 2006 respectively [22,23]. …”

Major evolutionary transitions and innovations: the tympanic middle ear

“…A tympanic ear is also present in most anurans (frogs and toads), although the Gymnophiona (such as the legless caecilians) and Caudata (salamanders) do not have tympanic ears. Some earless anurans are also found, where the body walls, mouth and lungs have been shown to serve as a route of sound transfer to the inner ear [1,2]. In reptiles and birds (the sauropsids), the middle ear space houses a single suspended ossicle, known as the stapes in reptiles and the columella in birds (figure 1 a ).…”

Acoustic analysis of the frequency-dependent coupling between the frog's ears

“…Monaural directivity patterns of the frog's ear have been measured (Chung et al, 1978(Chung et al, , 1981Feng, 1980;Rheinlaender, 1981;Pinder and Palmer, 1983;Jorgenson, 1991) and physiological evidence suggests that monaural directionality results from the interaction of multiple acoustic pathways to the ear (e.g., Feng and Shofner, 1981;Boistel et al, 2013;Lombard and Straughan, 1974;Wilczynski et al, 1987;Narins et al, 1988;Jorgensen, 1991). These studies were carried out under free-field conditions, and monaural directivity patterns have previously been modeled for these conditions (Fletcher and Thwaites, 1979;Palmer and Pinder, 1984;Aertson et al, 1986;Fletcher, 1992).…”