Directional Hearing and Head-Related Transfer Function in Odontocete Cetaceans.

The head-related transfer function (HRTF) is an important descriptor of spatial sound field reception by the listener. In this study, we computed the HRTF of the common dolphin Delphinus delphis. The received sound pressure level at various locations within the acoustic fats of the internal pinna near the surface of the tympanoperiotic complex (TPC) was calculated for planar incident waves directed toward the animal. The relative amplitude of the received pressure versus the incident pressure was the representation of the HRTF from the point of view of the animal. It is of interest that (1) different locations on the surface of the TPC resulted in different HRTFs, (2) the HRTFs for the left and right ears were slightly asymmetric, and (3) the locations of the peaks of the HRTF depended on the frequency of the incident wave.

Functional Morphology and Symmetry in the Odontocete Ear Complex.

Odontocete ear complexes or tympanoperiotic complexes (TPCs) were compared for asymmetry. Left and right TPCs were collected from one long-beaked common dolphin (Delphinus capensis) and one Amazon River dolphin (Inia geoffrensis). Asymmetry was assessed by volumetric comparisons of left and right TPCs and by visual comparison of superimposed models of the right TPC to a reflected mirror image of the left TPC. Kolmogorov-Smirnov tests were performed to compare the resonant frequencies of the TPCs as calculated by vibrational analysis. All analyses found slight differences between TPCs from the same specimen in contrast to the directional asymmetry in the nasal region of odontocete skulls.

Sound Transmission Validation and Sensitivity Studies in Numerical Models.

In 1974, Norris and Harvey published an experimental study of sound transmission into the head of the bottlenose dolphin. We used this rare source of data to validate our Vibroacoustic Toolkit, an array of numerical modeling simulation tools. Norris and Harvey provided measurements of received sound pressure in various locations within the dolphin's head from a sound source that was moved around the outside of the head. Our toolkit was used to predict the curves of pressure with the best-guess input data (material properties, transducer and hydrophone locations, and geometry of the animal's head). In addition, we performed a series of sensitivity analyses (SAs). SA is concerned with understanding how input changes to the model influence the outputs. SA can enhance understanding of a complex model by finding and analyzing unexpected model behavior, discriminating which inputs have a dominant effect on particular outputs, exploring how inputs combine to affect outputs, and gaining insight as to what additional information improves the model's ability to predict. Even when a computational model does not adequately reproduce the behavior of a physical system, its sensitivities may be useful for developing inferences about key features of the physical system. Our findings may become a valuable source of information for modeling the interactions between sound and anatomy.

Fin whale sound reception mechanisms: skull vibration enables low-frequency hearing.

Hearing mechanisms in baleen whales (Mysticeti) are essentially unknown but their vocalization frequencies overlap with anthropogenic sound sources. Synthetic audiograms were generated for a fin whale by applying finite element modeling tools to X-ray computed tomography (CT) scans. We CT scanned the head of a small fin whale (Balaenoptera physalus) in a scanner designed for solid-fuel rocket motors. Our computer (finite element) modeling toolkit allowed us to visualize what occurs when sounds interact with the anatomic geometry of the whale's head. Simulations reveal two mechanisms that excite both bony ear complexes, (1) the skull-vibration enabled bone conduction mechanism and (2) a pressure mechanism transmitted through soft tissues. Bone conduction is the predominant mechanism. The mass density of the bony ear complexes and their firmly embedded attachments to the skull are universal across the Mysticeti, suggesting that sound reception mechanisms are similar in all baleen whales. Interactions between incident sound waves and the skull cause deformations that induce motion in each bony ear complex, resulting in best hearing sensitivity for low-frequency sounds. This predominant low-frequency sensitivity has significant implications for assessing mysticete exposure levels to anthropogenic sounds. The din of man-made ocean noise has increased steadily over the past half century. Our results provide valuable data for U.S. regulatory agencies and concerned large-scale industrial users of the ocean environment. This study transforms our understanding of baleen whale hearing and provides a means to predict auditory sensitivity across a broad spectrum of sound frequencies.

Review of the cetacean nose: form, function, and evolution.

The cetacean nose presents a unique suite of anatomical modifications. Key among these is posterior movement of the external nares from the tip of the rostrum to the top of the head. Concomitant with these anatomical changes are functional changes including the evolution of echolocation in odontocetes, and reduction of olfaction in Neoceti (crown odontocetes and mysticetes). Anatomical and embryological development of the nose in crown cetaceans is reviewed as well as their functional implications. A sequence of evolutionary transformations of the nose is proposed in the transition from a terrestrial to an aquatic lifestyle made by whales. Basilosaurids and all later whales reduce the nasal turbinates. The next stage characterizes Neoceti which exhibit reduction of the major olfactory structures, i.e. the ethmoturbinates, cribriform plate and maxilloturbinates with further reduction and subsequent loss in odontocetes. These anatomical modifications reflect underlying genetic changes such as the reduction of olfactory receptor genes, although mysticetes retain some olfactory abilities. Modifications of the facial and nasal region of odontocetes reflect specialization for biosonar sound production.

Shape analysis of odontocete mandibles: functional and evolutionary implications.

Odontocete mandibles serve multiple functions, including feeding and hearing. We consider that these two major functions have their primary influence in different parts of the mandibles: the anterior feeding component and the posterior sound reception component, though these divisions are not mutually exclusive. One hypothesis is that sound enters the hearing apparatus via the pan bone of the posterior mandibles (Norris, Evolution and Environment,1968, pp 297-324). Another viewpoint, based on finite element models, suggests that sound enters primarily through the gular region and the opening created by the absent medial lamina of the posterior mandibles. This unambiguous link between form and function has catalyzed this study, which uses Geometric Morphometrics to quantify mandibular shape across all major lineages of Odontoceti. The majority of shape variation was found in the anterior (feeding) region: Jaw Flare (45.0%) and Symphysis Elongation (35.5%). Shape differences in the mandibular foramen, within the posterior (sound reception) region, also accounted for a small portion of the total variation (10.9%). The mandibles are an integral component of the sound reception apparatus in toothed whales and the geometry of the mandibular foramen likely plays a role in hearing. Furthermore, model goodness-of-fit tests indicate that mandibular foramina shapes, which appear conserved, evolved under a selective regime, possibly driven by sound reception requirements across Odontoceti.

Angular oscillation of solid scatterers in response to progressive planar acoustic waves: do fish otoliths rock?

Fish can sense a wide variety of sounds by means of the otolith organs of the inner ear. Among the incompletely understood components of this process are the patterns of movement of the otoliths vis-à-vis fish head or whole-body movement. How complex are the motions? How does the otolith organ respond to sounds from different directions and frequencies? In the present work we examine the responses of a dense rigid scatterer (representing the otolith) suspended in an acoustic fluid to low-frequency planar progressive acoustic waves. A simple mechanical model, which predicts both translational and angular oscillation, is formulated. The responses of simple shapes (sphere and hemisphere) are analyzed with an acoustic finite element model. The hemispherical scatterer is found to oscillate both in the direction of the propagation of the progressive waves and also in the plane of the wavefront as a result of angular motion. The models predict that this characteristic will be shared by other irregularly-shaped scatterers, including fish otoliths, which could provide the fish hearing mechanisms with an additional component of oscillation and therefore one more source of acoustical cues.

A new acoustic portal into the odontocete ear and vibrational analysis of the tympanoperiotic complex.

Global concern over the possible deleterious effects of noise on marine organisms was catalyzed when toothed whales stranded and died in the presence of high intensity sound. The lack of knowledge about mechanisms of hearing in toothed whales prompted our group to study the anatomy and build a finite element model to simulate sound reception in odontocetes. The primary auditory pathway in toothed whales is an evolutionary novelty, compensating for the impedance mismatch experienced by whale ancestors as they moved from hearing in air to hearing in water. The mechanism by which high-frequency vibrations pass from the low density fats of the lower jaw into the dense bones of the auditory apparatus is a key to understanding odontocete hearing. Here we identify a new acoustic portal into the ear complex, the tympanoperiotic complex (TPC) and a plausible mechanism by which sound is transduced into the bony components. We reveal the intact anatomic geometry using CT scanning, and test functional preconceptions using finite element modeling and vibrational analysis. We show that the mandibular fat bodies bifurcate posteriorly, attaching to the TPC in two distinct locations. The smaller branch is an inconspicuous, previously undescribed channel, a cone-shaped fat body that fits into a thin-walled bony funnel just anterior to the sigmoid process of the TPC. The TPC also contains regions of thin translucent bone that define zones of differential flexibility, enabling the TPC to bend in response to sound pressure, thus providing a mechanism for vibrations to pass through the ossicular chain. The techniques used to discover the new acoustic portal in toothed whales, provide a means to decipher auditory filtering, beam formation, impedance matching, and transduction. These tools can also be used to address concerns about the potential deleterious effects of high-intensity sound in a broad spectrum of marine organisms, from whales to fish.

Acoustic pathways revealed: simulated sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris).

The finite element modeling (FEM) space reported here contains the head of a simulated whale based on CT data sets as well as physical measurements of sound-propagation characteristics of actual tissue samples. Simulated sound sources placed inside and outside of an adult male Cuvier's beaked whale (Ziphius cavirostris) reveal likely sound propagation pathways into and out of the head. Two separate virtual sound sources that were located at the left and right phonic lips produced beams that converged just outside the head. This result supports the notion that dual sound sources can interfere constructively to form a biologically useful and, in fact, excellent sonar beam in front of the animal. The most intriguing FEM results concern pathways by which sounds reach the ears. The simulations reveal a previously undescribed 'gular pathway' for sound reception in Ziphius. Propagated sound pressure waves enter the head from below and between the lower jaws, pass through an opening created by the absence of the medial bony wall of the posterior mandibles, and continue toward the bony ear complexes through the internal mandibular fat bodies. This new pathway has implications for understanding the evolution of underwater hearing in odontocetes. Our model also provides evidence for receive beam directionality, off-axis acoustic shadowing and a plausible mechanism for the long-standing orthodox sound reception pathway in odontocetes. The techniques developed for this study can be used to study acoustic perturbation in a wide variety of marine organisms.

Anatomic geometry of sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris).

This study uses remote imaging technology to quantify, compare, and contrast the cephalic anatomy between a neonate female and a young adult male Cuvier's beaked whale. Primary results reveal details of anatomic geometry with implications for acoustic function and diving. Specifically, we describe the juxtaposition of the large pterygoid sinuses, a fibrous venous plexus, and a lipid-rich pathway that connects the acoustic environment to the bony ear complex. We surmise that the large pterygoid air sinuses are essential adaptations for maintaining acoustic isolation and auditory acuity of the ears at depth. In the adult male, an acoustic waveguide lined with pachyosteosclerotic bones is apparently part of a novel transmission pathway for outgoing biosonar signals. Substitution of dense tissue boundaries where we normally find air sacs in delphinoids appears to be a recurring theme in deep-diving beaked whales and sperm whales. The anatomic configuration of the adult male Ziphius forehead resembles an upside-down sperm whale nose and may be its functional equivalent, but the homologous relationships between forehead structures are equivocal.

Evaluation of postmortem changes in tissue structure in the bottlenose dolphin (Tursiops truncatus).

Postmortem changes in geometry, density, and sound speed within organs and tissues (melon, bone, blubber, and mandibular fat) of the dolphin head were evaluated using computed tomography (CT) scans of live and postmortem bottlenose dolphins (Tursiops truncatus). Specimens were classified into three different treatment groups: live, recently dead, and frozen followed by thawing. Organs and tissues in similar anatomical regions of the head were compared in CT scans of the specimens to identify postmortem changes in morphology. In addition, comparisons of Hounsfield units in the CT scans were used to evaluate postmortem changes in the density of melon, bone, blubber, and mandibular fat. Sound speed measurements from melon, blubber, connective tissue, and muscle were collected from fresh and frozen samples in the same specimen to evaluate effects due to freezing and thawing process on sound speed measurements. Similar results in tissue and organ geometry, density, and sound speed measurements suggested that postmortem material is a reliable approximation for live melon, bone, blubber, muscle, connective tissue, and mandibular fat. These results have implications for examining viscoelastic properties and the accuracy of simulating sound transmission in postmortem material.

Acoustic radiation from the head of echolocating harbor porpoises (Phocoena phocoena).

An experiment was conducted to investigate the sound pressure patterns on the melon of odontocetes by using four broadband hydrophones embedded in suction cups to measure echolocation signals on the surface of the forehead of two harbor porpoises (Phocoena phocoena). It has long been hypothesized that the special lipids found in the melon of odontocetes, and not in any other mammals, focus sounds produced in the nasal region that then propagate through the melon, producing a beam that is directional in both the horizontal and vertical planes. The results of our measurements supported the melon-focusing hypothesis, with the maximum click amplitude, representing the axis of the echolocation beam, located approximately 5.6-6.1 cm from the edge of the animal's upper lip along the midline of the melon. The focusing is not sharp but is sufficient to produce a transmission beam of about 16 degrees. Click amplitude dropped off rapidly at locations away from the location of site of maximum amplitude. Based on comparisons of forehead anatomy from similar sized porpoises, the beam axis coincided with a pathway extending from the phonic lips through the axis of the low-density/low sound velocity lipid core of the melon. The significant interaction between click number and hydrophone position suggests that the echolocation signals can take slightly different pathways through the melon, probably as a result of how the signals are launched by the production mechanism and the position of the acoustically reflective air sacs.

Cuvier's beaked whale (Ziphius cavirostris) head tissues: physical properties and CT imaging.

Tissue physical properties from a Cuvier's beaked whale (Ziphius cavirostris) neonate head are reported and compared with computed tomography (CT) X-ray imaging. Physical properties measured include longitudinal sound velocity, density, elastic modulus and hysteresis. Tissues were classified by type as follows: mandibular acoustic fat, mandibular blubber, forehead acoustic fat (melon), forehead blubber, muscle and connective tissue. Results show that each class of tissues has unique, co-varying physical properties. The mandibular acoustic fats had minimal values for sound speed (1350+/-10.6 m s(-1)) and mass density (890+/-23 kg m(-3)). These values increased through mandibular blubber (1376+/-13 m s(-1), 919+/-13 kg m(-3)), melon (1382+/-23 m s(-1), 937+/-17 kg m(-3)), forehead blubber (1401+/-7.8 m s(-1), 935+/-25 kg m(-3)) and muscle (1517+/-46.8 m s(-1), 993+/-58 kg m(-3)). Connective tissue had the greatest mean sound speed and density (1628+/-48.7 m s(-1), 1087+/-41 kg m(-3)). The melon formed a low-density, low-sound-speed core, supporting its function as a sound focusing organ. Hounsfield unit (HU) values from CT X-ray imaging are correlated with density and sound speed values, allowing HU values to be used to predict these physical properties. Blubber and connective tissues have a higher elastic modulus than acoustic fats and melon, suggesting more collagen structure in blubber and connective tissues. Blubber tissue elastic modulus is nonlinear with varying stress, becoming more incompressible as stress is increased. These data provide important physical properties required to construct models of the sound generation and reception mechanisms in Ziphius cavirostris heads, as well as models of their interaction with anthropogenic sound.