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Hearing and Age Estimation in Two Species of Arctic Whale

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Hearing and Age Estimation in Two Species of Arctic Whale HEARING AND AGE ESTIMATION IN TWO SPECIES OF ARCTIC WHALE A dissertation submitted to Kent State University in cooperation with Northeast Ohio Medical University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Jennifer Dawn Sensor August 2017 © Copyright All rights reserved Except for previously published materials Dissertation written by Jennifer Dawn Sensor B.S., Pennsylvania State University, 2008 Ph.D., Kent State University, 2017 Approved by J.G.M. Thewissen, Ph.D._________, Chair, Doctoral Dissertation Committee Jeffrey J. Wenstrup, Ph.D.________, Members, Doctoral Dissertation Committee Christopher J. Vinyard, Ph.D. ___ _ Lisa N. Cooper, PhD. __________ Mary Ann Raghanti, Ph.D.________ Accepted by Ernest J. Freeman, Ph.D._________, Director, School of Biomedical Sciences James L. Blank, Ph.D.___________, Dean, College of Arts and Sciences TABLE OF CONTENTS LIST OF FIGURES………………………………………………………………………….......v LIST OF TABLES...………………………………………………………………………….....ix PREFACE…………………………………………………………………………………….......x ACKNOWLEDGEMENTS………………………………………………………………….....xi CHAPTER I……………………………………………………………………………………...1 Evolution of the cetacean ear………….…..……………………………………………….4 Generalized hearing model…………....……………………………………………….......4 The outer ear of Cetacea…………………..……………………………………………….6 The middle ear of Cetacea…………………..……………………………………………..8 The inner ear of Cetacea…………………..……………………………………………...12 Communication and hearing in belugas…...……………………………………………...13 Communication and hearing in bowheads..……………………………………………...14 Under water anthropogenic sounds in the Arctic.………………………………………...14 Age estimation in bowheads…..…………..……………………………………………...16 Summary of the dissertation……………………………………………………………..17 CHAPTER II……………………………………………………………………………………19 The spiral ganglion and Rosenthal’s canal of beluga whales Introduction.……………………………………………………………………………...20 Materials and Methods.…………………………………………………………………..24 Results……………………………………………………………………………………39 Discussion………………………………………………………………………………..41 Conclusions………………………………………………………………………………48 iii CHAPTER III…………………………………………………………………………………..49 Spiral ganglion and Rosenthal’s canal in a low-frequency baleen whale: the bowhead whale Introduction……………………………………………………………………………....50 Materials and Methods…………………………………………………………………...52 Results……………………………………………………………………………………59 Discussion………………………………………………………………………………..61 Conclusions………………………………………………………………………………70 CHAPTER IV…………………………………………………………………………………...72 Age estimation in bowhead whales using tympanic bulla histology and baleen isotopes Introduction…………………………………………………………………....................73 Materials and Methods…………………………………………………………………...74 Results……………………………………………………………………………………78 Discussion………………………………………………………………………………..89 Conclusions………………………………………………………………………………96 CHAPTER V……………………………………………………………………………………98 Concluding Remarks Contributions to the field………………………………………………………………..106 Future directions……….………………………………………………………………..106 REFERENCES………………………………………………………………………………...109 iv LIST OF FIGURES Figure 1.1…………………………………………………………………………………………2 Distribution map of bowhead and beluga whales Figure 1.2.......................................................................................................................................3 The spiral ganglion and Rosenthal’s canal of beluga and bowhead Figure 1.3………………………………………………………………………………...……….7 Sound reception pathway for modern land mammals versus odontocetes Figure 1.4…………………………………………………………………………………………9 Representative views of the petro-tympanic complex of odontocetes and mysticetes Figure 2.1………………………………………………………………………………………..27 Delphinapterus leucas microCT scan Figure 2.2………………………………………………………………………………………..28 Delphinapterus leucas AMIRA3-D reconstructions of bony labyrinth and spiral ganglion Figure 2.3………………………………………………………………………………………..30 Delphinapterus leucas specimen dissection and preparation Figure 2.4………………………………………………………………………………………..32 Delphinapterus leucas petrosal showing anatomy and different stages of dissection Figure 2.5………………………………………………………………………………………..34 Delphinapterus leucas cochlear segment map Figure 2.6………………………………………………………………………………………..35 Delphinapterus leucas spiral ganglion histological sections of specimen 2010LDL21 Right v Figure 2.7………………………………………………………………………………………..37 Delphinapterus leucas, three variables of the spiral ganglion plotted against their cochlear position Figure 2.8………………………………………………………………………………………..45 Natural logarithm of spiral ganglion counts and basilar membrane length versus body weight for several cetaceans. Figure 2.9.………………………………………………………………………………………47 Delphinapterus leucas, number of ganglion cells in segments of the spiral ganglion against mean histological cross-sectional area of that segment Figure 3.1………………………………………………………………………………………..54 Balaena mysticetus boney anatomy and microCT scan Figure 3.2………………………………………………………………………………………..55 Balaena mysticetus AMIRA3-D reconstructions of cochlea and Rosenthal’s canal Figure 3.3………………………………………………………………………………………..56 Balaena mysticetus, three variables of the spiral ganglion plotted against their position along the cochlea Figure 3.4………………………………………………………………………………………..58 Balaena mysticetus cochlear segment map of 2012B18R Figure 3.5………………………………………………………………………………………..62 Balaena mysticetus, spiral ganglion histological sections specific distances from the base Figure 3.6………………………………………………………………………………………..63 Balaena mysticetus, enlarged histological image of specimen 2010B15R vi Figure 3.7………………………………………………………………………………………..69 Balanena mysticetus, number of ganglion cells in segments of the spiral ganglion against mean histological cross-sectional area of that segment Figure 4.1……………………………………………………………………………………......75 Balaena mysticetus, the tympanic bulla Figure 4.2……………………………………………………………………………………......81 Balaena mysticetus, baleen isotope signatures and tympanic GLGs for multiple whales Figure 4.3……………………………………………………………………………………......82 Balaena mysticetus, baleen isotope signature and tympanic GLGs for whale NSB-DWM 2013B18 Figure 4.4……………………………………………………………………………………......83 Balaena mysticetus, baleen isotope signature and tympanic GLGs of whale NSB-DWM 2011B9 Figure 4.5……………………………………………………………………………………......84 Balaena mysticetus, baleen isotope signature and tympanic GLGs of whale NSB-DWM 2013B1 Figure 4.6……………………………………………………………………………………......85 Balaena mysticetus, region 3 microstructure of six tympanic bone slices under brightfield magnification Figure 4.7……………………………………………………………………………………......86 Balaena mysticetus, region 3 of two whale specimens displaying GLG variability Figure 4.8………………………………………………………………………………………..88 δ13C signatures of tympanic bone and baleen transects vii Figure 4.9………………………………………………………………………………………..91 Tympanic bulla GLG counts plotted against four other variables from these same bowhead individuals Figure 5.1……………………………………………………………………………………....100 Three variables of the spiral ganglion plotted against their position along the cochlea Figure 5.2………………………………………………………………………………………102 Attenuation of sound in fresh and sea water, dB per km and Hz (Denny 1993) Figure 5.3………………………………………………………………………………………104 Natural logarithm of spiral ganglion counts and basilar membrane length versus natural logarithm of body weight for several cetaceans and terrestrial mammals Figure 5.4………………………………………………………………………………………108 GLGs in the periosteal region of the tympanic bone of fossil Eocene whale, Nalacetus viii LIST OF TABLES Table 2.1..………………………………………………………………………………………..26 Date of sampling, sex, length, and relative age of beluga whales used in this inner ear study Table 2.2........................................................................................................................................43 Species, number of cochlear whorls, basilar membrane length (mm) and estimated spiral ganglion neuron number for several odontocete species Table 3.1………………………………………………………………………………...…….....65 Morphometric data and number of neurons in the spiral ganglion for multiple mysticete whales Table 3.2..………………………………………………………………………………………..68 Biological data on the bowheads used in this inner ear study Table 4.1…………………………………………………………………………………………79 Estimated parameters for the von Bertalanffy II growth model of Lubetkin et al. (2012) Table 4.2…………………………………………………………………………………………90 List of bowhead whale specimens used in this age estimation study Table 5.1………………………………………………………………………………………103 Approximate body weight, basilar membrane length, and number of spiral ganglion neurons in multiple mysticetes, odontocetes, and terrestrial mammals ix PREFACE Chapters I and V of this document are original material written for the purpose of the dissertation. Chapter II was originally published as a research article in the Journal of Morphology in 2015. Contributing authors are Jennifer D. Sensor (myself), R. Suydam, J. C. George, M. C. Liberman, D. Lovano, M. A. Rhaganti, S. Usip, C. J. Vinyard, and J. G. M. Thewissen. J.G.M. Thewissen and I designed the research and wrote the paper, and all contributing authors performed the research and/or analyzed the data. Chapter IV was has been accepted for publication in Marine Mammal Science. Contributing authors are Jennifer D. Sensor (myself), J. C. George, M.T. Clementz, D. M. Lovano, D. A. Waugh, G. H. Givens, R. Suydam, R. Stimmelmayr, and J. G. M. Thewissen. J.G.M. Thewissen and I designed the research, all contributing authors performed the research and/or analyzed that data, and J.G.M Thewissen, M.T. Clementz, G.H. Givens, and I wrote
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