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Cetacean Ears Hearing by Whales &N'u Edirors: Richard R

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Cetacean Ears Hearing by Whales &N'u Edirors: Richard R Whitlow WL. Au Whitlow w.l. Au Arthw N. Popper Arthur N. Popper Marine Mammal Research Program Department of Biology and Richard R. Fay Hawaii Inslitule of Marine Biology Newoscienc:e and Cognitive Science Un..iv~rsity of Hawa'i Program Editors Kailua, HI 96734, USA University of Maryland Richard R. Fay CoUege Park, MD 20742, USA 2 Parmly Hearing In,titute and Deparlment or P,ychoLogy LoyoLa University of Olicago Chicago, IL 60626, USA Cetacean Ears Hearing by Whales &n'u Edirors: Richard R. Fay and Arthur N. Popper and Dolphins DARLENE R. KETIEN Cov.er:: The image i; a 3D reconstruction (rom cr scans of a left inner ear of an adllkmaJe Cuvier's beaked w:h lie (Ziph,us CQ'Vitostrisj. The image shows the ear from -I. !alen'll ....:iew wich Ibe facial :nerve an the- fOTeground, The auditory nerve caDa] Bod cochlear canals arejust above and ~hind che faciaJ nerve. Phbto courtesy Df Darlene: R. Kenco. With 152 ILlustralions Libra.ry of Cong:ress CatalogiJlg-in-Publication Data He.a.ring by whales and dolphins' [edited by] 'Whitlow Au, Arthur N. Popper, Richard R. Fay. p. cm.-(Springer fJ8t1dbook 01 auditory research) Jodudes- bibliottspbical (·dereoces.. ISDN 0-387·94\106.2 (bardcmer ,oIt. pape<) I. Dolphi Pby>iology. 2. Whales-PhysioLogy. 3. H"rin~ :v.~~tlo W.L. Ii. Popper, Arthur N. Ill. Fay, Richard R. QL737.C432H42S 2000 S73.1r9L9.5-dc21 9'1-40947 Printed on. acid-free paper. 1. Introduction €;I 20(0 Springer.Vertag New York IDe.. AU righ IS resen:ed. Th.!- work may oct be translated or copied in whole or in part without the Whales and dolphins are majestic elusive, charismatic creatures that couple written penniSSJOD oC Ib<: publli;her (Springer.VerJag New YOfk, Inc.. 175 FrClh A\'enue. New t ':ork.~ .0010.U?A), ~:l'Cept {<If brief ~-cerpts i~ connedion wifh review3 orscholarly analy. Si~ Use m connection waLlI any fonn (If mformatlon ItOTa,g.e and reCrieval. e1ectronK: adap'a­ exceptional grace with enormous power. These features may account for tWll, computer softwaTe., or by simUar Qr dissimilar lJlC:thodol.C)gy now known -or here-uter developed is forbidden. much of humanity's enduring fascination with whales, but they are terrible ~e use 01 g.eneral descriptiy-e na.mes,. .lnd.c .Dames., Uademarks,. etc.. In this. publication. even If the former are. not espeaaUy idellhfl..ed. lIS not to be taken as a sign lbal such names. as understood bf tbe Tt3dc Mara a.rtd Me.rclandi.se Marks Act. may acoordincJlr be used fred,.­ reasons for studying their auditory systems.The principal reason whale ears byanyo-ne. are worth investigating is ... Ginger Rogers. Ginger Rogers and Fred ProouctlOI\ managed boy Terry Komak; maDufacturing npervised by Erica B~1e.r. Typeset by Dest-set ~pesetter Ltd., Hong Kon~ P~nted ~nd bound by Maple-Vail Book ManUfacturing Group, York, PA. Astaire were a famous dance team. Mr. Astaire was renowned for his grace Printed m l:he Uni(ed S1ates (Jf America. Springe, and agility. What people rarely note is that Ms. Rogers not only matched 9876 S ~ 32 l i her partl\er step for step, she did it wearing a cumbersome gown, in high ISBN 0-387-94906-2 Sprln:eer-V-eflil,£. New Y(Jlk Berlin HeideU:JCJ~ SPIN mS:581D4 heels, and backwards. Just as Ginger kept pace with Fred but in a different orientation and with added burdens, whales hear as well as land mammals but in a different medium with special acoustic burdens. This chapter provides an overview of the anatomical foundation of whale hearing. It takes a functional, comparative approach, emphasizing how structures unique to peripheral auditory systems in the two extant subor­ ders of Cetacea, the Odontoceti (toothed whales, porpoises, and dolphins) and Mysticeti (rorqualsand baleen whales) relate to the ability of a mam­ malian ear to hear in water. Commonalities with land mammal ears are dis­ cussed in terms of their significance for fundamental hearing mechanisms. Anatomical specializations found across land mammal, odontocete, and mysticete ears are discussed in terms of the role they play in determining species-specific frequency ranges as adaptations to cross-media behaviors and niche substructure. The primary task of this chapter is to deconstruct whale and dolphin ears to determine which elements are simply mammalian and which are aquatic or devoted to special acoustic tasks. The concept that there is a significant relationship between ear structure and hearing capacity, and that both are related to the animal's niche, is par,ticularly relevant for understanding whale hearing. Analyzing how hearing capacity and auditory structures covary in a range of species can provide important insights into funda­ mental 'hearing mechanisms that take place in the auditory periphery 44 D.R. Ketten 2. Cetacean Ears 45 (Fay 1992). If we extend the analyses to ultra- and infrasonic animals, we employ the broadest known acoustic range, spanning low infrasonic (10Hz) can learn substantially more about how hearing ranges are determined as to high ultrasonic (200 kHz) frequencies. well as how to detect and use physical cues that are normally impercepti­ Hearing is arguably the primary sensory and communication channel for ble to us (e.g., Hinchcliffe and Pye 1968; Webster and Webster 1975). Using cetaceans, and we expect all whale ears are highly evolved. Comparative ears adapted to different media, we can begin to explore how the auditory functional anatomy studies may be the only way to understand the breadth system deals with physical features of acoustic cues. of whale ears because the majority of whale species are not approachable Whales and dolphins fit all three criteria for productive analyses. Even by conventional audiometry. Only about 13% of all species have ever been more important, cetacean ears are derived from land mammal auditory tested, all those tested are from one suborder, and nearly all are from one systems but may now be more acoustically and physically diverse than any family. Given the diversity of habitats, behaviors, and sizes that cetaceans related land mammal group. Whales originally had air-adapted ears. All encompass, it would be naive to expect that data from a few species or one cetaceans are descended from mesonychid condylarths, catlike, carnivorous, division will provide a full picture of cetacean hearing. By analyzing the land-based ungulates that became amphibious in the Eocene, probably to structure ofa broad spectrum ofcetacean ears, we can gain insights not only exploit food-rich near-shore waters (Thewissen 1998). In the intervening 50 into whale hearing and aquatic adaptations but also into some basic hearing to 60 million years, as these condylarths gradually transformed from hoofed issues. First, similarities between land and aquatic mammal ears are likely waders into full-fledged, flippered whales, every portion of their anatomy to be related to fundamental mammalian ear mechanisms. Second, struc­ was physically and functionally reshaped to accommodate life in water. tures that are common among aquatic species but lacking or significantly Their air-adapted high-frequency mammalian· ears had to be coupled to different in land mammals are probably key elements for transducing water-borne sound for hearing to remain functional, but ear'evolution took water-borne sound. Third, because of extreme variations among whales in place in tandem with other body reconfigurations. Just as the physical animal size, sound use patterns, and habitats, differences that we see among demands ofoperat.ing in water exacted a structural price in the locomotory whale and dolphin ears that have land mammal parallels can teach us some­ and t~rmoregulatory systems of marine mammals, the physics of swim­ thing about how auditory anatomy is shaped by physiologic and environ­ ming, diving, and resting on the sudace reshaped the head. Modem mental factors. cetaceans have the most derived cranial structure of any mammal (Thewis­ Therefore, the most cogent reason for studying whale ears is simply to sen 1998; Cranford, Chapter 3). "Telescoping," a term coined by Miller find out how they to do it, that is, how do they hear-at high speed, under (1923), refers to the evolutionary revamping of the cetacean face. As the pressure, and underwater. anterior cranial structures pushed up and back, one bone sliding over another, every facet of the auditory periphery was modified: pinnae and external auditory canals were lost, the middle and inner ear capsules fused, 2. Comparative Acoustics: Sound in Air Versus Water and a new ear complex with the bone density of enamel erupted from its intracranial position to settle into a newly formed, cavernous peribulLar To understand ears, it is imperative to understand not only how they were sinus. Today, all cetaceans are absolute aquatics, unable to move, reproduce, evolutionarily tailored by the fundamental needs ofthe animal but also how or feed on land, and their ears are so fully adapted to water-borne sound the information options were constrained by the acoustic properties of the that they may no longer be able to detect or interpret airborne signals. Con­ medium in which each species evolved. To properly assess whale ears and sequently they have ancestral ear elements in common with land mammals place them in a general mammalian hearing context,· it is necessary to but have added hydro-related specializations that hold clues to media­ understand how the physical properties of water vs. air affect acoustic cues. dependent hearing mechanisms. Because water is denser than air, sound in water travels faster and with Currently, there are 76 extant species of whales, ranging in size from less attenuation than sound in air. Sound speed (c) in moist ambient sudace the harbor porpoise (Phocoena phocoena, 1m, 55 kg) to the blue whale air is approximately 34Om/s.
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