Abstract
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.
Highlights
The current paper addresses several questions related to the odontocete hearing structure/function complex: 1) What are the probable sites and mechanisms for acoustic stimulation of the tympanoperiotic complex (TPC)? 2) Is the ossicular chain functional? 3) If so, how might sound pressure be transmitted through the TPC to the cochlea as vibrational motions or displacements?
We examined the gross morphology of the gular anatomy and the mandibular fat body (MFB) in more than 25 odontocete species using hand dissection and remote imaging techniques like computed tomography (CT) and MR scanning
Despite the research papers that question the function of the ossicular chain in odontocetes [13,20,51], we present evidence based on morphology and modeling results suggesting that ossicular motion is integral to the function of the TPC
Summary
Ethics Statement Postmortem toothed whale specimens for this project were obtained from five sources: National Marine Fisheries Service (NMFS), Navy Marine Mammal Program (NMMP), SeaWorld San Diego, Portland State University, and the National Museum of Natural History at the Smithsonian Institution. The San Diego State University Institutional Animal Care and Use Committee (IACUC) has reviewed and approved our methods for handling, dissecting, and disposal of postmortem marine mammal tissue samples. Their approval was issued in a document (APF# 09-05014B) entitled, ‘‘Marine Mammal Dissections’’ and is dated 17 June 2009. Over the past twenty years, one of us (Cranford) has studied xray computed tomography (CT) scans from more than 30 species of odontocetes [30,31,32]. The large size of the specimens and advancements in CT technology has dictated that the exact imaging parameters for specimens have necessarily changed over the years. The parameters employed were always sufficient to discriminate the smallest structures of interest
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