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.

[1]  K. S. Norris,et al.  a Theory for the Function of the Spermaceti Organ of the Sperm Whale (physeter Catodon L) , 1972 .

[2]  John A. Hildebrand,et al.  Lagrangian finite element treatment of transient vibration/acoustics of biosolids immersed in fluids , 2008 .

[3]  U. Varanasi,et al.  Unique lipids of the porpoise (Tursiops gilli): differences in triacyl glycerols and wax esters of acoustic (mandibular canal and melon) and blubber tissues. , 1971, Biochimica et biophysica acta.

[4]  P E Nachtigall,et al.  Echolocation signals and transmission beam pattern of a false killer whale (Pseudorca crassidens). , 1995, The Journal of the Acoustical Society of America.

[5]  J. Lilly Man and Dolphin , 1962 .

[6]  Laura N. Kloepper,et al.  Active echolocation beam focusing in the false killer whale, Pseudorca crassidens , 2012, Journal of Experimental Biology.

[7]  S. Ridgway,et al.  Nasal Pressure and Sound Production in an Echolocating White Whale, Delphinapterus leucas , 1988 .

[8]  A. J. Greenberg,et al.  Comparative lipid patterns in the melon fats of dolphins, porpoises and toothed whales , 1974 .

[9]  W. Au,et al.  Dolphin biosonar signals measured at extreme off-axis angles: insights to sound propagation in the head. , 2011, The Journal of the Acoustical Society of America.

[10]  K. S. Norris Some problems of echolocation in cetaceans , 1964 .

[11]  U. Varanasi,et al.  Molecular basis for formation of lipid sound lens in echolocating cetaceans , 1975, Nature.

[12]  K. S. Norris Peripheral Sound Processing in Odontocetes , 1980 .

[13]  W. Au,et al.  The acoustic field on the forehead of echolocating Atlantic bottlenose dolphins (Tursiops truncatus). , 2008, The Journal of the Acoustical Society of America.

[14]  K. S. Norris,et al.  Sound transmission in the porpoise head. , 1974, The Journal of the Acoustical Society of America.

[15]  Whitlow W. L. Au,et al.  The Sonar of Dolphins , 1993, Springer New York.

[16]  Hans-Ulrich Schnitzler,et al.  Echolocation signals of a beaked whale at Palmyra Atoll. , 2010, The Journal of the Acoustical Society of America.

[17]  Wesley R. Elsberry,et al.  Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): Evidence for two sonar sources , 2011 .

[18]  R. W. Baird,et al.  Characterization of Marine Mammal Recordings from the Hawaii Range Complex , 2010 .

[19]  Robert E Shadwick,et al.  Cuvier's beaked whale (Ziphius cavirostris) head tissues: physical properties and CT imaging , 2005, Journal of Experimental Biology.

[20]  S. Rommel,et al.  Vascularization of Air Sinuses and Fat Bodies in the Head of the Bottlenose Dolphin (Tursiops truncatus): Morphological Implications on Physiology , 2012, Front. Physio..

[21]  A. J. Greenberg,et al.  Compositional topography of melon lipids in the amazon river dolphin, inia geoffrensis: Implications for echolocation , 1979 .

[22]  D. A. Pabst,et al.  Morphology of the melon and its tendinous connections to the facial muscles in bottlenose dolphins (Tursiops truncatus) , 2008, Journal of morphology.

[23]  B. Würsig,et al.  The Hawaiian Spinner Dolphin , 1994 .

[24]  Mats Amundin,et al.  Sound production in odontocetes, with emphasis on the harbour porpoise, Phocoena phocoena , 1991 .

[25]  W. Au,et al.  Transmission beam pattern and echolocation signals of a harbor porpoise (Phocoena phocoena). , 1999, The Journal of the Acoustical Society of America.

[26]  W. E. Evans,et al.  Mechanisms of Sound Production in Delphinid Cetaceans: A Review and some Anatomical Considerations , 1973 .

[27]  L. Miller,et al.  Sperm whale clicks: directionality and source level revisited. , 2000, The Journal of the Acoustical Society of America.

[28]  The Study of the Sound Production Apparatus in the Harbour Porpoise, Phocoena Phocoena , and the Jacobita, Cephalorhynchus Commersoni by Means of Serial Cryo-Microtome Sectioning and 3-D Computer Graphics , 1988 .

[29]  J. Lilly,et al.  Sounds Emitted by the Bottlenose Dolphin , 1961, Science.

[30]  P. Krysl,et al.  A New Acoustic Portal into the Odontocete Ear and Vibrational Analysis of the Tympanoperiotic Complex , 2010, PloS one.

[31]  P. Moore,et al.  Frequency-dependent variation in the two-dimensional beam pattern of an echolocating dolphin , 2011, Biology Letters.

[32]  Mardi C. Hastings,et al.  Echolocation in Marine Mammals , 2008 .

[33]  G. Miller The telescoping of the cetacean skull (with eight plates) , 1923 .

[34]  Julie N Oswald,et al.  A tool for real-time acoustic species identification of delphinid whistles. , 2005, The Journal of the Acoustical Society of America.

[35]  Marc O Lammers,et al.  The beluga whale produces two pulses to form its sonar signal , 2009, Biology Letters.

[36]  R. W. Floyd,et al.  Propagation of Atlantic bottlenose dolphin echolocation signals , 1978 .

[37]  Patrick W. Moore,et al.  Investigations on the Control of Echolocation Pulses in the Dolphin (Tursiops Truncatus) , 1990 .

[38]  Mikael Evander,et al.  An echolocation visualization and interface system for dolphin research. , 2008, The Journal of the Acoustical Society of America.

[39]  P. Moore,et al.  Beamwidth control and angular target detection in an echolocating bottlenose dolphin (Tursiops truncatus). , 2008, The Journal of the Acoustical Society of America.

[40]  T. Cranford The Anatomy of Acoustic Structures in the Spinner Dolphin Forehead as Shown by X-Ray Computed Tomography and Computer Graphics , 1988 .

[41]  U. Varanasi,et al.  Triacylglycerols Characteristic of Porpoise Acoustic Tissues: Molecular Structures of Diisovaleroylglycerides , 1972, Science.

[42]  A. Gaunt,et al.  Electromyographic and Pressure Events in the Nasolaryngeal System of Dolphins during Sound Production , 1980 .

[43]  Whitlow W. L. Au,et al.  Echolocation in dolphins and bats , 2007 .

[44]  W. E. Evans Echolocation by marine delphinids and one species of fresh‐water dolphin , 1973 .

[45]  C. Hoh,et al.  Structural and functional imaging of bottlenose dolphin (Tursiops truncatus) cranial anatomy , 2004, Journal of Experimental Biology.

[46]  Nachum Ulanovsky,et al.  Active Control of Acoustic Field-of-View in a Biosonar System , 2011, PLoS biology.

[47]  P. Nachtigall,et al.  Single-lobed frequency-dependent beam shape in an echolocating false killer whale (Pseudorca crassidens). , 2012, The Journal of the Acoustical Society of America.

[48]  Margaret L. Brandeau,et al.  Optimal Localization by Pointing Off Axis , 2010 .

[49]  T. Cranford,et al.  Functional morphology and homology in the odontocete nasal complex: Implications for sound generation , 1996, Journal of morphology.

[50]  J. Mead Anatomy of the External Nasal Passages and Facial Complex in the Delphinidae (Mammalia: Cetacea) , 1975 .

[51]  J. Shilling Man and Dolphin , 1961 .

[52]  Marie A Roch,et al.  Classification of Risso's and Pacific white-sided dolphins using spectral properties of echolocation clicks. , 2008, The Journal of the Acoustical Society of America.

[53]  C. Clark,et al.  Communication and Acoustic Behavior of Dolphins and Whales , 2000 .

[54]  Bertel Møhl,et al.  Sound transmission in the nose of the sperm whale Physeter catodon. A post mortem study , 2001, Journal of Comparative Physiology A.

[55]  R. Morris The lipid structure of the spermaceti organ of the sperm whale (Physeter catodon) , 1973 .

[56]  A. J. Greenberg,et al.  Compositional topography of melon lipids in the Atlantic bottlenosed dolphin Tursiops truncatus: Implications for echo-location , 1973 .

[57]  J. Dilger,et al.  Physical factors influencing refraction of the echolocative sound beam in delphinid cetaceans , 1979 .

[58]  T. Cranford,et al.  Forehead Anatomy of Phocoena Phocoena and Cephalorhynchus Commersonii : 3-Dimensional Computer Reconstructions with Emphasis on the Nasal Diverticula , 1990 .

[59]  J. Hildebrand,et al.  Evaluation of postmortem changes in tissue structure in the bottlenose dolphin (Tursiops truncatus) , 2007, Anatomical record.

[60]  Kenneth S. Norris,et al.  Computer modeling of acoustic beam formation in Delphinus delphis , 1992 .

[61]  P W Moore,et al.  Echolocation transmitting beam of the Atlantic bottlenose dolphin. , 1986, The Journal of the Acoustical Society of America.

[62]  M. McKenna,et al.  Morphology of the odontocete melon and its implications for acoustic function , 2012 .

[63]  J. Hildebrand,et al.  Gaussian mixture model classification of odontocetes in the Southern California Bight and the Gulf of California. , 2007, The Journal of the Acoustical Society of America.

[64]  H. Riquimaroux,et al.  Adaptive beam-width control of echolocation sounds by CF–FM bats, Rhinolophus ferrumequinum nippon, during prey-capture flight , 2013, Journal of Experimental Biology.

[65]  S. Iverson,et al.  High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon , 2003, Journal of Comparative Physiology B.

[66]  Ted W. Cranford,et al.  THE SPERM WHALE'S NOSE: SEXUAL SELECTION ON A GRAND SCALE?1 , 1999 .

[67]  Kenneth S. Norris,et al.  AN EXPERIMENTAL DEMONSTRATION OF ECHOLOCATION BEHAVIOR IN THE PORPOISE, TURSIOPS TRUNCATUS (MONTAGU) , 1961 .

[68]  K. S. Norris,et al.  Behavior of the Hawaiian Spinner Dolphin 'Stenella longirostris' (Schlegel, 1841). , 1979 .

[69]  Petr Krysl,et al.  Acoustic pathways revealed: simulated sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris) , 2008, Bioinspiration & biomimetics.

[70]  James J Finneran,et al.  Directional properties of bottlenose dolphin (Tursiops truncatus) clicks, burst-pulse, and whistle sounds. , 2012, The Journal of the Acoustical Society of America.

[71]  Cetacean Behavior: Mechanisms and Functions, Louis M. Herman (Ed.). John Wiley, New York (1980), xiii , 1981 .

[72]  H. Oelschläger Evolutionary Morphology and Acoustics in the Dolphin Skull , 1990 .

[73]  Mackay Rs,et al.  Dolphin vocalization mechanisms. , 1981 .

[74]  W. Au,et al.  The biosonar field around an Atlantic bottlenose dolphin (Tursiops truncatus). , 2012, The Journal of the Acoustical Society of America.

[75]  rdens Djurpark,et al.  BONY NARES AIR PRESSURE AND NASAL PLUG MUSCLE ACTIVITY DURING CLICK PRODUCTION IN THE HARBOUR PORPOISE , PHOCOENA PHOCOENA , AND THE BOTTLENOSED DOLPHIN , TURSIOPS TRUNCATUS , 2005 .

[76]  D. K. Caldwell,et al.  Compositional topography of melon and spermaceti organ lipids in the pygmy sperm whale Kogia breviceps: Implications for echolocation , 1978 .

[77]  J. Prescott,et al.  Observations of the sound production capabilities of the bottlenose porpoise: A study of whistles and clicks , 1962, Zoologica : scientific contributions of the New York Zoological Society..

[78]  R. Morris Further studies into the lipid structure of the spermaceti organ of the sperm whale (Physeter catodon) , 1975 .

[79]  Kenneth J. Dormer,et al.  Mechanism of sound production and air recycling in delphinids: Cineradiographic evidence , 1979 .

[80]  Petr Krysl,et al.  Anatomic geometry of sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris). , 2008, Anatomical record.

[81]  P. Madsen,et al.  Single source sound production and dynamic beam formation in echolocating harbour porpoises (Phocoena phocoena) , 2010, Journal of Experimental Biology.

[82]  R S Mackay,et al.  Dolphin vocalization mechanisms. , 1981, Science.

[83]  D. K. Caldwell,et al.  Comparative lipid patterns in acoustical and nonacoustical fatty tissues of dolphins, porpoises and toothed whales. , 1975, Comparative biochemistry and physiology. B, Comparative biochemistry.

[84]  U. Varanasi,et al.  Role of isovaleroyl lipids in channeling of sound in the porpoise melon. , 1982, Chemistry and physics of lipids.

[85]  Vera M. Ostrovskaya,et al.  Organization of Communication System in Tursiops Truncatus Montagu , 1990 .

[86]  Biosonar sources in odontocetes: considering structure and function , 2011, Journal of Experimental Biology.

[87]  Kenneth S. Norris,et al.  The Porpoise Watcher , 1974 .

[88]  Hans-Ulrich Schnitzler,et al.  Discriminating features of echolocation clicks of melon-headed whales (Peponocephala electra), bottlenose dolphins (Tursiops truncatus), and Gray's spinner dolphins (Stenella longirostris longirostris). , 2010, The Journal of the Acoustical Society of America.

[89]  Ted W. Cranford,et al.  In Search of Impulse Sound Sources in Odontocetes , 2000 .

[90]  H. Oelschläger Morphological and functional adaptations of the toothed whale head to aquatic life , 2000 .

[91]  P. Krysl,et al.  Angular Oscillation of Solid Scatterers in Response to Progressive Planar Acoustic Waves: Do Fish Otoliths Rock? , 2012, PloS one.

[92]  Robert J. Urick,et al.  Principles of underwater sound , 1975 .

[93]  S.M. Wiggins,et al.  High-frequency Acoustic Recording Package (HARP) for broad-band, long-term marine mammal monitoring , 2007, 2007 Symposium on Underwater Technology and Workshop on Scientific Use of Submarine Cables and Related Technologies.