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Acoustics Australia

, Volume 45, Issue 2, pp 273–278 | Cite as

The Tympanal Recess of the Cetacean Cochlea: Function and Evolution

  • Travis Park
  • Erich M. G. Fitzgerald
  • Alistair R. Evans
Original Paper

Abstract

Cetaceans (whales and dolphins) primarily use sound to communicate and hunt for prey. Their auditory anatomy is highly specialised, but much about its function remains unknown. In particular, a feature of the cochlea known as the tympanal recess present in some mysticetes (baleen whales) and odontocetes (toothed whales) has defied functional explanation. Here, we present and discuss several hypotheses that may clarify the function and evolution of the tympanal recess. One potential function in particular, the vibroacoustic duct mechanism, seems most plausible although further work is needed to test the hypothesis, which hints at the possibility of sperm whales and beaked whales being able to detect both high and low frequencies.

Keywords

Cetacea Cochlea Hearing Tympanal recess Vibroacoustic duct mechanism Frequency 

Introduction

In adapting to an aquatic mode of life, cetaceans (whales and dolphins) have come to rely on auditory cues to hunt and/or communicate, with the senses of smell and vision reduced due to the physical properties of water [1]. The hearing of both living groups of cetaceans (baleen whales and toothed whales) is extremely specialised (although it should be noted there are as yet no audiograms for mysticetes), with sound waves entering the cetacean auditory pathway via unique acoustic fat pads and/or bone conduction of the skull depending on the group [2, 3, 4] and a highly inflated tympanic bulla in the middle ear. However, similar to terrestrial mammals, sound is ultimately detected in the inner ear (the cochlea) when a pressure differential is created between the scala media and the scala tympani (Fig. 1). This differential displaces the cochlear hair cells, stimulating neurons that signal to the brain a sound has been detected [5]. The cochlea therefore is the final arbiter in determining what sounds an animal can hear; with the shape and structure of the cochlea influencing what frequencies it can actually detect [6]. Novel structures in the cochlea are therefore of interest as they may determine hearing abilities.
Fig. 1

Cross section of a generalised mammalian cochlear canal showing distribution of structures and scalae

Fig. 2

Digital endocasts and microCT cross-sectional slices of cochleae of A, Platanista gangetica (NMV C27417) and B, Tasmacetus shepherdi (NMV C37967), illustrating the absence and presence of a tympanal recess, respectively. Digital endocasts are from Park et al. [14, Fig S4] and cross-sectional slices were taken from the microCT scan dataset of Park et al. [14]

One such structure is the radial expansion of the scala tympani, also known as the tympanal recess (Fig. 2). This feature appears to be an apomorphy of Neoceti (Mysticeti + Odontoceti). Despite Fleischer [7] reporting a substantial tympanal recess in the sperm whale Physeter macrocephalus, Ekdale [8] and Ekdale and Racicot [9] state that the feature is only present in balaenopteroids (balaenopterids + eschrichtiids) and the extinct cetotheriid Herpetocetus. More recent research has also identified the feature in the fossil mysticetes Metopocetus,Piscobalaena and Cephalotropis as well as an indeterminate early odontocete and toothed mysticete [10, 11]. However, following the definition of the tympanal recess given in Park et al. [12], where any radial expansion of the scala tympani that exceeds the basal quarter turn is classed as a tympanal recess, we do not consider there to be a tympanal recess in the toothed mysticete cochlea figured by Ekdale [11, Fig. 3].We have also recently confirmed that a distinct tympanal recess not only occurs in the taxa mentioned above, but also in the pygmy right whale Caperea marginata [13] and in several odontocetes (Physeter and beaked whales of the family Ziphiidae) [14] (Fig. 3). This scattered distribution across Neoceti has thus far confounded potential functional explanations of its evolution as the taxa that possess the feature are distantly related and appear to possess disparate hearing abilities. Here we discuss several hypotheses on the function of the tympanal recess, what has potentially driven its evolution and lay out the future steps that need to be taken to investigate the matter further.

Potential Function of the Tympanal Recess

Reduction in Hydrodynamic Distortion

Fleischer [7] hypothesised that an expanded scala tympani reduces hydrodynamic distortion at high sound intensities in the cochlear fluid. Whilst this could help explain how cetacean ears can handle the extremes in wavelengths and intensities that they have become specialised for, it does not account for the fact that some taxa lack a tympanal recess and yet also encounter the same sound intensities [15].

Focusing Acoustic Energy

An earlier study [6] showed there is a strong relationship between low frequency hearing and the graded curvature of the cochlea (although the sample was mainly comprised of terrestrial mammals), where the ratio of the radii of curvature from the basal and apical turns of the cochlear spiral is inversely proportional to the low frequency limit. Increasing the basal radius of the cochlea will therefore increase the value of this ratio, allowing the animal to detect lower frequencies. It might appear, therefore, that this increase in the basal radius could theoretically be achieved by an expansion of the scala tympani (i.e. a tympanal recess). Whilst this appears to make sense, the physical pathway that an incoming sound takes within the inner ear makes this impossible. Sound waves travel to the apex of the cochlea via the scala vestibuli, pass through the helicotrema and then back down the cochlear spiral along the scala tympani (Fig. 4a). Therefore, expanding the scala tympani will not help to focus acoustic energy towards the top of the cochlea as the vibrations are travelling in the wrong direction.
Fig. 3

Phylogeny of cetacean families, with those that possess a tympanal recess marked in red. Phylogeny is a composite of Ekdale [11], McGowen et al. [30] and Marx and Fordyce [31]. ChM stands for Charleston Museum vertebrate palaeontology collection

Fig. 4

Schematic view of the tympanoperiotic complex demonstrating alternative routes of cochlear stimulation. a the traditional pathway where vibrations of the tympanic bulla (1) set the middle ear ossicles into motion (2). The sound then travels to the cochlear apex via the scala vestibuli (3) before returning to the base via the scala tympani (4); b the vibroacoustic mechanism where vibrations travel along the perilymphatic duct (1) and travel to the cochlear apex via the scala tympani (2) and returns to the base via the scala vestibuli (3). Image modified from March et al. [16]

Vibroacoustic Duct Mechanism

A hypothetical solution to the problem of acoustic energy travelling the wrong direction in the cochlea for the tympanal recess to focus it is a novel route of cochlear stimulation known as the vibroacoustic duct mechanism, which was first proposed by March et al. [16]. Rather than sound waves reaching the cochlea via the middle ear bones in the traditional manner, the vibroacoustic duct mechanism instead transmits acoustic energy to the cochlea via the perilymphatic duct, entering the cochlea through the canaliculus cochleae (Fig. 4). Vibrations will therefore travel to the cochlea apex via the scala tympani rather than the scala vestibuli, meaning that having a tympanal recess would be useful for focusing acoustic energy towards the apex (see sect. 2.2). Whilst not all mysticete clades possess a tympanal recess, it is interesting to note that those that do not (i.e. balaenids) have more loosely coiled cochlear apices [11], perhaps using this morphology to achieve a similar effect as that of the tympanal recess. This mechanism therefore presents an alternative pathway for low frequency sounds to reach the cochlea, especially given that low frequency sound waves are not sufficiently strong as an excitation mechanism on the tympanoperiotic complex for wavelengths longer than the body of the animal [4]. For example, for an animal 5 m in length, any sound waves with a frequency lower than 320 Hz will not have an effect on the tympanoperiotic complex. In mysticetes in particular, the vibroacoustic duct mechanism would complement hypotheses of bone conduction, where acoustic energy is transmitted to the tympanoperiotic complex by vibration of the skull itself.

March et al. [16] initially proposed the vibroacoustic duct mechanism for a ziphiid, based on its hypertrophied canaliculus cochleae. Interestingly, it has also been noted that physeterids and ziphiids retain a bony connection to the skull through a pneumatised posterior process [4, 16]. Combining these observations with the fact that Physeter and ziphiids also possess a tympanal recess, there is the intriguing possibility that these odontocetes are also capable of detecting low frequencies using the bone conduction and vibroacoustic duct mechanisms. This hypothesis remains untested at present.

Evolutionary Drivers of the Tympanal Recess

Body Size

It is possible that the tympanal recess is a result of the evolution of the extreme body size seen in most modern mysticetes, with the scala tympani disproportionately expanding in size as the animals became larger. Whilst this could account for the evolution of the feature in balaenopteroids and physeterids which reach lengths of 33 and 16 m, respectively [17], it does not explain the development of a tympanal recess in the much smaller C. marginata, Gray’s beaked whale Mesoplodon grayi and Shepherd’s beaked whale Tasmacetus shepherdi. Size does not appear to be the driving factor, unless these relatively small extant taxa have inherited and retained a tympanal recess from larger-bodied ancestors.

Dive Depth

An expanded scala tympani could be an adaptation that allows the cochlea to function at extreme depth, which in physeterids and ziphiids can be 2000 and 3000 m, respectively [18, 19]. This, however, does not explain the presence of the tympanal recess in baleen whales, which do not dive further than 350 m [20]. Furthermore, some odontocete taxa such as the pygmy sperm whale Kogia breviceps dive deeper (up to 1200 m [21]) than mysticete taxa that possess a tympanal recess, yet do not possess a tympanal recess themselves.

Feeding Ecology

Could the manner in which a cetacean feeds influence cochlear morphology and drive the evolution of the tympanal recess? Another part of the auditory pathway has been previously linked with specialisations in feeding ecology. Yamato and Pyenson [22] found that balaenopteroids possess laterally facing acoustic funnels and parallel tympanic bullae, linking this morphology to the specialised lunge-feeding seen in rorquals. Interestingly, a common feature of the feeding of taxa that possess a tympanal recess is a rapid opening of the mouth, with balaenopterids being lunge feeders [23, 24, 25] and eschrichtiids, physeterids and ziphiids being suction feeders. All taxa with a tympanal recess have some form of throat grooves thought to increase the capacity of the oral cavity. Crucially, in odontocetes, only sperm whales and beaked whales possess this feature [26, 27]. Exactly what the link between possessing throat grooves and rapidly opening your mouth and having tympanal recess remains unclear, although it may be related to any sudden change in pressure level within the cochlear fluid or the pressure differential between the cochlea and middle ear cavity of these animals as they rapidly open their mouths. The exception to this hypothesis, however, is the pygmy right whale Caperea marginata. This species, which is most likely a cetotheriid (although not all studies agree), possesses throat grooves like all other tympanal recess-possessing taxa. However, it skim-feeds like balaenids, a method that does not employ a rapid opening of the oral cavity or generation of suction. However, it may be the case that the tympanal recess in C. marginata is a result of phylogenetic constraint. Evidence for this comes from the fact that other cetotheriids, which possessed a tympanal recess (e.g. Herpetocetus), were also thought to have employed lateral suction feeding in a manner analogous to eschrichtiids [11, 28] and that its disparate feeding ecology relative to other cetotheriids allowed it to survive when the rest of the lineage went extinct [29].

Conclusions and Future Work

The tympanal recess, a radial expansion of the scala tympani, is a cochlear feature that appears to be unique to cetaceans. Its broad (seemingly random) phylogenetic distribution has vexed illumination of its function. Here, we have collated and discussed potential functions of the tympanal recess and what could have driven its evolution. The majority of the hypotheses presented above all have clear exceptions to them that make them unlikely to be the main driver. One hypothesis, the vibroacoustic duct mechanism, however, remains plausible although untested. The tympanal recess may be a new piece of evidence for the novel route of cochlear stimulation in cetaceans first proposed by March et al [16]. The potential implication of this hypothesis if supported is that some odontocetes may be able to detect both high and low frequencies. Whilst the taxa implicated here (Physeter and ziphiids) have cochleae that are clearly adapted to detecting high frequencies, it is also worthwhile noting that their secondary spiral laminae are the shortest of any extant odontocetes (based on the sample of Park et al. [14]). This implies that they would have a more flexible apical end of the basilar membrane and may therefore be more receptive to lower frequencies than other odontocetes. Additional evidence of a possible ability to detect low frequencies is the high radii ratio values recorded for ziphiids and Physeter. This ratio, which is negatively correlated with low frequency limit, shows that the ziphiids and Physeter specimens from the sample of Park et al. [14] are 9.60, 8.5 and 4.91, respectively. These values would suggest an increased sensitivity to low frequencies in these taxa; indeed the values recorded for ziphiids are as high as those found for mysticetes.

In terms of future work, the following steps should be taken to explore the tympanal recess further and test the viability of the vibroacoustic duct mechanism hypothesis: (1) Dissections should be made of the auditory region of taxa that possess a tympanal recess to determine the anatomy of the perilymphatic duct and surrounding area; (2) Comparative dissections should also be made of the same area in taxa that lack a tympanal recess to check for differences/similarities; (3) As noted by March et al. [16], the impedance of the perilymphatic duct should be calculated so that its ability to transfer vibrational energy can be determined; and (4) comparative histological sections should be made of cetacean cochleae with the aim of determining the exact soft tissue structure of the tympanal recess.

Notes

Acknowledgements

We thank Karen Roberts, Katie Date and David Pickering (Museums Victoria) for access to Museums Victoria collections, as well as Will Gates (Monash University X-ray Microscopy Facility for Imaging Geo-materials) and Rob Williams (Melbourne Brain Centre Imaging Unit) for their help in digitising the specimens. Felix Marx (Monash University) is also thanked for helpful discussions. This research was supported by an Australian Research Council Linkage Project LP150100403 to A.R.E. and E.M.G.F.

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Copyright information

© Australian Acoustical Society 2017

Authors and Affiliations

  1. 1.School of Biological SciencesMonash UniversityMelbourneAustralia
  2. 2.GeosciencesMuseums VictoriaMelbourneAustralia
  3. 3.National Museum of Natural HistorySmithsonian InstitutionWashingtonUSA
  4. 4.Department of Life SciencesNatural History MuseumLondonUK

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