1Sound is the primary sensory cue for most marine mammals, and this is especially true for 2 cetaceans. To passively and actively acquire information about their environment, cetaceans 3 have perhaps the most derived ears of all mammals, capable of sophisticated, sensitive hearing 4 and auditory processing. These capabilities have developed for survival in an underwater world 5 where sound travels five times faster than in air, and where light is quickly attenuated and often 6 limited at depth, at night, and in murky waters. Cetacean auditory evolution has capitalized on 7 the ubiquity of sound cues and the efficiency of underwater acoustic communication. The sense 8 of hearing is central to cetacean sensory ecology, enabling vital behaviors such as locating prey, 9 detecting predators, identifying conspecifics, and navigating. Increasing levels of anthropogenic 10 ocean noise appears to influence many of these activities. 11Here we describe the historical progress of investigations on cetacean hearing, with a 12 particular focus on odontocetes and recent advancements. While this broad topic has been 13 studied for several centuries, new technologies in the last two decades have been leveraged to 14 improve our understanding of a wide range of taxa, including some of the most elusive species. 15 This paper addresses topics including how sounds are received, what sounds are detected, 16 hearing mechanisms for complex acoustic scenes, recent anatomy and physiology studies, the 17 potential impacts of noise, and mysticete hearing. We conclude by identifying emerging 18 research topics and areas which require greater focus. 19 20 3

Cetaceans possess highly derived auditory systems adapted for underwater hearing. Odontoceti (toothed whales) are thought to receive sound through specialized fat bodies that contact the tympanoperiotic complex, the bones housing the middle and inner ears. However, sound reception pathways remain unknown in Mysticeti (baleen whales), which have very different cranial anatomies compared to odontocetes. Here, we report a potential fatty sound reception pathway in the minke whale (Balaenoptera acutorostrata), a mysticete of the balaenopterid family. The cephalic anatomy of seven minke whales was investigated using computerized tomography and magnetic resonance imaging, verified through dissections. Findings include a large, well-formed fat body lateral, dorsal, and posterior to the mandibular ramus and lateral to the tympanoperiotic complex. This fat body inserts into the tympanoperiotic complex at the lateral aperture between the tympanic and periotic bones and is in contact with the ossicles. There is also a second, smaller body of fat found within the tympanic bone, which contacts the ossicles as well. This is the first analysis of these fatty tissues' association with the auditory structures in a mysticete, providing anatomical evidence that fatty sound reception pathways may not be a unique feature of odontocete cetaceans. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.

Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

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Like elephants, baleen whales produce low-frequency (LF) and even infrasonic (IF) signals, suggesting they may be particularly susceptible to underwater anthropogenic sound impacts. Analyses of computerized tomography scans and histologies of the ears in five baleen whale and two elephant species revealed that LF thresholds correlate with basilar membrane thickness/width and cochlear radii ratios. These factors are consistent with high-mass, low-stiffness membranes and broad spiral curvatures, suggesting that Mysticeti and Proboscidea evolved common inner ear adaptations over similar time scales for processing IF/LF sounds despite operating in different media.

The lack of baleen whale (Cetacea Mysticeti) audiograms impedes the assessment of the impacts of anthropogenic noise on these animals. Estimates of audiograms, which are difficult to obtain behaviorally or electrophysiologically for baleen whales, can be made by simulating the audiogram as a series of components representing the outer, middle, and inner ear (Rosowski, 1991;Ruggero and Temchin, 2002). The middle-ear portion of the system can be represented by the middle-ear transfer function (METF), a measure of the transmission of acoustic energy from the external ear to the cochlea. An anatomically accurate finite element model of the minke whale (Balaenoptera acutorostrata) middle ear was developed to predict the METF for a mysticete species. The elastic moduli of the auditory ossicles were measured by using nanoindentation. Other mechanical properties were estimated from experimental stiffness measurements or from published values. The METF predicted a best frequency range between approximately 30 Hz and 7.5 kHz or between 100 Hz and 25 kHz depending on stimulation location. Parametric analysis found that the most sensitive parameters are the elastic moduli of the glove finger and joints and the Rayleigh damping stiffness coefficient b. The predicted hearing range matches well with the vocalization range.

18 2In an underwater environment where light attenuates much faster than in air, cetaceans 19 have evolved to rely on sound and their sense of hearing for vital functions. Odontocetes 20 (toothed whales) have developed a sophisticated biosonar system called echolocation, allowing 21 them to perceive their environment using their sense of hearing (Schevill and McBride 1956, 22 Kellogg 1958, Norris et al. 1961). Echolocation has not been demonstrated in mysticetes (baleen 23 whales). However, mysticetes rely on low frequency sounds, which can propagate very long 24 distances under water, to communicate with potential mates and other conspecifics (Cummings 25 and Thompson 1971). 26The mechanism of sound reception in cetaceans has been debated for centuries. 27Cetaceans have lost the external pinna and the ear canal has also been reduced to a narrow, increased separation between the skull and ears is thought to reduce bone conduction, aiding 32 directional hearing under water (Claudius 1858, in Yamada 1953, van Heel 1962. 33In the 1960's, the "jaw hearing" hypothesis was proposed for odontocete cetaceans 34 (Norris 1964). Odontocetes possess unusual mandibles, which have enlarged mandibular hiatuses 35 filled with discrete fat bodies that are in direct contact with the tympano-periotic complex. These 36 fats also cover the outer parts of the mandible in most species. It had been noted earlier that 37 physical properties of sound in water are similar to those in most body tissues (Reysenbach de 38 Haan 1957), so the ear canal is not well-suited for underwater sound reception. However, Norris 39 suggested that the fat bodies associated with the mandibles act as a preferential pathway for 40 sound to get from the aquatic environment to the ears because "fat especially is closely 41 3 impedance-matched to sea water" (Norris 1968). While the detailed mechanisms are still unclear, 42Norris's theory has been subsequently validated by behavioral, physiological, and anatomical 43 studies (e.g., Bullock et al. 1968, Brill et al. 1988, Ketten 2000. 44The "acoustic fats" involved with odontocete sound reception are an example of a 45 structural fatty tissue, as opposed to a storage tissue. Whereas the volume and lipid composition 46 of storage fat, such as human abdominal fat and marine mammal blubber, generally change with 47 body condition and diet, structural fats, such as those found in the feet, joints, and eye sockets, 48are metabolically inert and do not expand during obesity or shrink during fasting (Pond 1998). 49These structural fats contain fewer dietary components than storage tissues. The fatty melon in 50 the odontocete forehead, which is part of the high frequency sound transmission pathway during 51 echolocation, is another structural "acoustic fat" in odontocetes. Cranford et al. (1996) noted that 52 the melon remains intact even in emaciated animals, and Koopman et al. (2003) showed that the 53 lipid content and fatty acid (FA) composition of the melon is stable across body conditions, 54wh...

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