Ted W. Cranford

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 Cuviers 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.

Computer modeling of acoustic beam formation in Delphinus delphis

It has been established that some dolphins possess well‐developed acoustic orientation (echolocation) and information gathering abilities, though substantially less is known about the system of sound generation and beam formation. Dolphins use a narrowly focused sound beam that emanates from the forehead and rostrum during echolocation. The primary objectives of this study were to simulate the effects of anatomical structure on beam formation, and to test the viability of various hypothetical sound source locations. Outlines from parasagittal x‐ray CT scans were used to construct a 2‐D model of the head of the common dolphin, Delphinus delphis. Finite difference techniques were used to simulate sound propagation through tissues modeled as inhomogeneous fluids. Preliminary simulations confirm that beam formation results primarily from reflection off of the skull and the skull‐supported air sac surfaces. For the frequencies tested, beam angles best approximate those measured by experimental methods for a so...

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

SUMMARY Tissue physical properties from a Cuviers 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.

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

SUMMARY 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 animals upper lip along the midline of the melon. The focusing is not sharp but is sufficient to produce a transmission beam of about 16°. 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.

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.

Validation of a vibroacoustic finite element model using bottlenose dolphin simulations: the dolphin biosonar beam is focused in stages

Psychoacoustic laboratory studies with live dolphins require considerable resources and are essential for assessing the validity of our models. Computerized numerical modelling methods are a reasonable approach to simulate the vibroacoustic functions of the dolphin biosonar apparatus. In order to validate this approach, we chose a vibroacoustic finite element model to simulate sound production and sound beam formation in the bottlenose dolphin (Tursiops truncatus), based on computed tomography scans from live and postmortem dolphins. The right and left dorsal bursae were assumed to be potential sound sources. The simulations confirm several hypotheses: (1) the shape of the skull plays a role in the formation of the sound transmission beam; (2) the melon appears to concentrate the acoustic energy by a factor of four in the transmitted beam; (3) focusing the sound beam apparently occurs in a series of stages that include contributions from the skull, nasal diverticula, melon and connective tissue structures. An unexpected result is that adjustments to the focus and direction of the sound beam can result from small (millimetre scale) changes in the relative position of the anterior and posterior bursae within each sound generation complex. Comparing our results with those from dolphin psychoacoustic experiments establishes validation of our vibroacoustic model. The potential for varied effects from anthropogenic sound also emphasizes the importance of developing vibroacoustic modelling. These numerical modelling tools complement experimental data for determining exposure thresholds and may allow us to simulate exposure levels, from moderate to extreme, without impacting live animals.

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. Anat Rec, 290:1023–1032, 2007.

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. Anat Rec, 297:2205–2215, 2014.

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. J. Morphol.

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.