Histological and ultrastructural aspects of the nasal complex in the Harbour Porpoise, Phocoena phocoena

Journal of Morphology

Volumn 270, Issue 11, 2009, Pages 1320-1337

  Prahl, Susanne ^a   Huggenberger, Stefan ^b   Schliemann, Harald ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Bio sonar; Cetacea; Mechanoreceptor; Odontoceti; Phonic lips; Sound generation

Indexed keywords

ANIMAL; ARTICLE; ATMOSPHERIC PRESSURE; AUDIOVISUAL EQUIPMENT; HISTOLOGY; NOSE CAVITY; PORPOISE; SKULL; ULTRASTRUCTURE; VOCALIZATION;

AIR PRESSURE; ANIMALS; MODELS, ANATOMIC; NASAL CAVITY; PHOCOENA; SKULL; VOCALIZATION, ANIMAL;

CETACEA; ODONTOCETI; PHOCOENA; PHOCOENA PHOCOENA; PHOCOENIDAE;

EID: 70350714903     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10760     Document Type: Article

References (82)

1. Amundin M, Andersen SH. 1983. Bony nares air pressure and nasal plug muscle activity during click production in the harbour porpoise, Phocoena phocoena, and the bottlenosed dolphin, Tursiops truncatus. J Exp Biol 105:275-282.
2. Amundin M, Cranford TW. 1990. Forehead anatomy of Phocoena Phocoena and Cephalorhynchus commersonii: 3-dimensional computer reconstructions with emphasis on the nasal diverticula. In: Thomas JA, Kastelein RA, editors. Sensory Abilities of Cetaceans. New York: Plenum Press, Plenum Publishing Corporation. pp 1-18.
3. Aroyan J, McDonald M, Webb S, Hildebrand J, Clark D, Laitman J, Reidenberg J. 2000. Acoustic models of sound production and propagation. In: Au W, Popper A, Fay R, editors. Hearing by Whales and Dolphins. New York: Springer. pp 409-470.
4. Au WWL. 1993. The Sonar of Dolphins. Berlin: Springer. 277 p.
5. Au WWL, Kastelein RA, Benoit-Bird KJ, Cranford TW, McKenna MF. 2006. Acoustic radiation from the head of echolocating harbor porpoises (Phocoena phocoena). J Exp Biol 209:2726-2733.
6. Bryden MM, Molyneux GS. 1986. Ultrastructure of encapsulated mechanoreceptor organs in the region of the nares. In: Harrison RJ, editor. Research on Dolphins. Oxford: Clarendon Press. pp 99-107.
7. Buhl EH, Oelschlager HA. 1986. Ontogenetic development of the nervus terminalis in toothed whales. Anat Embryol 173:285-294.
8. Comtesse-Weidner P. 2007. Untersuchungen am Kopf des fetalen Narwals Monodon monoceros Ein Atlas zur Entwicklung und funktionellen Morphologie des Sonarapparates [Dissertation]. Gießen: Justus-Liebig-Universitat. 204 p.
9. Cranford TW. 2000. Search of impulse sound sources in odontocetes. In: Au W, Popper A, Fay R, editors. Hearing in Whales and Dolphins. New York: Springer. pp 109-155.
10. Cranford TW, Amundin M. 2004. Biosonar pulse production in odontocetes: The state of our knowledge. In: Thomas JA, Moss C, Vater M, editors. Echolocation in Bats and Dolphins. Chicago: University Press. pp 26-59.
11. Cranford TW, Amundin M, Norris KS. 1996. Functional morphology and homology in the odontocete nasal complex: Implications for sound generation. J Morph 228:223-285.
12. Cranford TW, Van Bonn WG, Chaplin MS, Carr JA, Kamolnick TA, Carder DA, Ridgway S. 1997. Visualizing dolphin sonar signal generation using high speed video endoscopy. J Acoust Soc Am 102:3123.
13. Cranford TW, Krysl P, Hildebrand JA. 2008a. Acoustic pathways revealed: simulated sound transmission and reception in Cuvier's beaked whale (Ziphius cavirostris). Bioinsp Biomim (Bioinspiration & Biomimetics) 3,:doi:10.1088/1748-3182/ 1083/1081/016001.
14. Cranford TW, McKenna MF, Soldevilla MS, Wiggins SM, Goldbogen JA, Shadwick RE, Krysl P, Leger JA, Hildebrand JA. 2008b. Anatomic geometry of sound transmission and reception in Cuvier's Beaked Whale (Ziphius cavirostris). Anat Rec 291:353-378.
15. Curry BE. 1992. Facial anatomy and potential function of facial structures for sound production in the harbor porpoise (Phocoena phocoena) and Dall's porpoise (Phocoenoides dalli). Can J Zool 70:2103-2114.
16. Danciu TE, Gagari E, Adam RM, Damoulis PD, Freeman MR. 2004. Mechanical strain delivers anti-apoptotic and proliferative signals to gingival fibroblasts. J Dent Res 83:596-601.
17. Degollada E, Garcia Hartmann M, Lammers M. 1996. A role for nasal pigmentation in odontocete species. In: Evans PGH, editor. Proceedings of the Tenth Annual Conference of the European Cetacean Society. Lisbon, Portugal: Vol. 10. pp 309-310.
18. Degollada E, Hartmann MG, Cranford TW. 1998. Histological structure of the sound generation complex in delphinoid cetaceans. In: Evans PGH, Parsons ECM, editors. Proceedings of the Twelfth Annual Conference of the European Ceta-cean Society, Monaco. p 298.
19. Dormer KS. 1979. Mechanism of sound production and air recycling in delphinids: Cineradiographic evidence. J Acoust Soc Am 65:229-239.
20. Dudok van Heel WH. 1981. Investigations on Cetacean Sonar III. A Proposal for an Ecological Classification of Odontocetes in Relation with Sonar. Aquat Mamm 8:65-68.
21. Evans WE, Maderson PFA. 1973. Mechanisms of sound production in delphinid cetaceans: A review and some anatomical considerations. Am Zool 13:1205-1213.
22. Fordyce RE, Muizon C. de. 2001. Evolutionary history of the cetaceans: A review. In: Mazin J-M, de Buffrénil V, editors. Secondary Adaptation of Tetrapods to Life in Water. Munchen: Verlag r. Friedrich Pfeil. pp 169-234.
23. Gaskin DE. 1976. The evolution, zoogeography and ecology of cetacea. Oceanogr Mar Biol Ann Rev 14:247-346.
24. Geraci JR, St Aubin DJ, Hicks BD. 1986. The epidermis of odontocetes: a view from within. In: Bryden MM, Harrison R, editors. Research on Dolphins. Oxford: Clarendon Press. pp 3-21.
25. Geneser F. 1990. Histologie. Koln: Deutscher Ärzteverlag. 800 p.
26. Goodson AD, Flint JA, Cranford TW. 2004. The harbor porpoise (Phocoena phocoena)-Modeling the sonar transmission mechanism. In: Thomas JA, Moss C, Vater M, editors. Echolocation in Bats and Dolphins. Chicago: University Press. pp 64-72.
27. Gruhl K. 1911. Beitrage zur Anatomie und Physiologie der Cetaceennase. [Inaugural-Disseration zur Erlangung der philosophischen Doktorwurde der Hohen Philosophischen Fakul-tat der Koniglichen Universitat Breslau]. Breslau: Konigliche Universitat Breslau. pp 1-49.
28. Haldiman JT, Henk WG, Henry RW, Albert TF, Abdelbaki YZ, Duffield DW. 1985. Epidermal and papillary dermal characteristics of the bowhead whale (Balaena mysticetus). Anat Rec 211:391-402.
29. Harrison RJ, Thurley KW. 1974. Structure of the epidermis in Tursiops, Delphinus, Orcinus and Phocoena. In: Harrison RJ, editor. Functional Anatomy of Marine Mammals. London: Academic Press. pp 45-71.
30. Heyning JE. 1989. Comparative facial anatomy of beaked whales (Ziphiidae) and a systematic revision among the fami-lies of extant odontoceti. Contrib Sci 405:1-64.
31. Heyning JE, Mead JG. 1990. Evolution of the nasal anatomy of Cetaceans. In: Thomas JA, Kastelein RA, editors. Sensory Abilities of Cetaceans. New York: Plenum Publishing Corporation. pp 67-79.
32. Huggenberger S, Rauschmann MA, Vogl TJ, Oelschlager HHA. 2009. Functional morphology of the nasal complex in the harbor porpoise (Phocoena phocoena L.) Anat Rec, doi: 10.1002/ar.20854.
33. Jacobs MS, Morgane PJ, McFarland WL. 1971. The Anatomy of the brain of the Bottlenose Dolphin (Tursiops truncatus). Rhinic Lobe (Rhinencephalon). I. Palaeocortex. J Comp Neu-rol 141:205-272.
34. Kellogg WN. 1958. Echo ranging in the Porpoise: Perception of objects by reflected sound is demonstrated for the first time in marine animals. Science 128:982-988.
35. Klima M. 1987. Morphogenesis of the nasal structures of the skull in toothed whales (Odontoceti). In: Kuhn HJ, Zeller U, editors. Morphogenesis of the Mammalian Skull. Hamburg: Paul Parey. pp 105-121.
36. Klima M. 1999. Development of the cetacean nasal skull. Adv Anat Embryol Cell Biol 149:1-143.
37. Klima M, Breev, PJH. 1985. Überzahlige Skeletelemente im Nasenschadel von Phocoena phocoena und die Entwicklung der Nasenregion bei den Zahnwalen. Gegenbaurs morph Jahrb, Leipzig 131:131-178.
38. Knospe C. 1989. Zur Wasseranpassung der Walhaut. Anat Histol Embryol 18:193-198.
39. Kolchin SP, Belkovich VM. 1973. Tactile sensitivity in Delphinus delphis. Zoologisceskiy Zhurnal 52:620-622.
40. Kukenthal W. 1893. Vergleichend-Anatomische und Entwickelungsgeschichtliche Untersuchungen an Walthieren. Denkschriften der Medicinisch-Naturwissenschaftlichen Gesellschaft zu Jena 3:322-349.
41. Lawrence B, Schevill WE. 1956. The functional anatomy of the delphinid nose. Bull Mus Comp Zool 114:103-197.
42. Liebich HG. 1990. Funktionelle Histologie. Farbatlas und Kurzlehrbuch der mikroskopischen Anatomie der Haussaugetiere. Ed. 2, Schattauer. pp 1-353.
43. Mackay RS, Liaw HM. 1981. Dolphin Vocalization Mechanisms. Science 212:676-678.
44. Mead JG. 1975. Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia: Cetacea). Smithson Contrib Zool 207:1-72.
45. Menon GK, Grayson S, Brown BE, Elias PM. 1986. Lipokeratinocytes of the epidermis of a cetacean (Phocena phocena). Cell Tissue Res 244:385-394.
46. Miller GS. 1923. The telescoping of the cetacean skull. Smithson Misc Collect 76:1-71.
47. Norris KS. 1964. Some problems of echolocation in cetaceans. In: Tavolga UN, editor. Marine Bio-Acoustics. Oxford: Pergamon Press. pp 317-336.
48. Norris KS. 1968: The evolution of acoustic mechanisms in odontocete cetaceans. In: Drake ET, editor. Evolution and Environment. New Haven: Yale University Press. pp 297-324.
49. Norris KS. 1975. Cetacean biosonar. I. Anatomical and behavioral studies. In: Malins DC, Sargent JR, editors. Biochemical and Biophysical Perspectives in Marine Biology. New York: Academic Press. pp 215-236.
50. Norris KS. 1980. Peripheral sound processing in odontocetes. In: Busnel RG, Fish JF, editors. Animal Sonar Systems. New York: Plenum Press. pp 495-509.
51. Norris KS, Harvey GW. 1974. Sound transmission in the porpoise head. J Acoust Soc Am 56:659-664.
52. Norris KS, Prescott JH, Asa-Dorian PV, Perkins P. 1961. An experimental demonstration of echolocation behaviour in the Porpoise. Tursiops truncatus (Montagu) Biol Bull 120:163-176.
53. Norris KS, Dormer KJ, Pegg J, Liese GJ. 1971. The mechanism of sound production and air recycling in porpoises: A preliminary report. Proceedings of the VIII Conf. Biol. Sonar Diving Mammals, Menlo Park, CA. Stanford Research Institute. pp 113-129.
54. Nummela S, Hussain ST, Thewissen JGM. 2006. Cranial anatomy of Pakicetidae (Cetacea. Mammalia). J Verteb Palaeontol 26:746-759.
55. Oelschlager HA. 1990. Evolutionary morphology and acoustics in the dolphin skull. In: Thomas J, Kastelein R, editors. Sensory Abilities of Cetaceans. New York: Plenum Press. pp 137-162.
56. Oelschlager HA. 1992. Development of the olfactory and terminalis systems in whales and dolphins. In: Doty RL, Muller-Schwarze D, editors. Chemical Signals in Vertebrates VI. New York: Plenum Press. pp 141-147.
57. Oelschlager HA, Buhl EH. 1985a. Occurrence of an olfactory bulb in the early development of the harbor porpoise (Phocoena phocoena L.). In: Duncker/Fleischer, editor. Fortschritte der Zoologie. Stuttgart: Gustav Fischer Verlag. pp 695-698.
58. Oelschlager HA, Buhl EH. 1985b. Development and rudimentation of the peripheral olfactory system in the harbor porpoise Phocoena phocoena (Mammalia: Cetacea). J Morph 184: 351-360.
59. Oelschlager HA, Kemp B. 1998. Ontogenesis of the sperm whale brain. J Comp Neurol 399:210-228.
60. Palmer E, Weddell G. 1964. The relationship between structure, innervation and function of the skin of the bottle nose dolphin (Tursiops truncatus). Proc Zool Soc Lond 143:553-568.
61. Pfeiffer CJ, Menon GK. 2002. Cellular ultrastructural and biochemical specializations in the cetacean epidermis. In: Pfeiffer CJ, editor. Molecular and Cell Biology of Marine Mammals. Malabar, Florida: Krieger Publishing Company. pp 396-411.
62. Prahl S. 2007. Untersuchungen zum Bau der epicranialen Atemwege beim Schweinswal (Phocoena phocoena Linnaeus, 1758). Doctoral Thesis, Department of Zoology, University of Hamburg. (http://www.sub.uni-hamburg.de/opus/volltexte/2007/3456/).
63. Purves PE, Pilleri GE. 1983. Echolocation in whales and dolphins. London: Academic Press. pp 1-261.
64. Rauschmann MA, Huggenberger S, Kossatz LS, Oelschlager HA. 2006. Head morphology in perinatal dolphins: A window into phylogeny and ontogeny. J Morph 267:1295-1315.
65. Raven HC, Gregory WK. 1933. The spermaceti organ and nasal passages of the sperm whale (Physeter catodon) and other odontocetes. Am Mus Novitates: Vol. 677, pp 1-18.
66. Rawitz B. 1900. Die Anatomie des Kehlkopfes und der Nase von Phocaena communis Cuv. Intern Monatsschr Anat und Physiol 17:245-354.
67. Reidenberg JS, Laitman JT. 2008. Sisters of the sinuses: cetacean air sacs. Anat Rec 291:1389-1396.
68. Ridgway SH, Carder DA, Green RF, Gaunt AS, Gaunt SLL, Evans WE. 1980. Electromyographic and pressure events in the nasolaryngeal system of dolphins during sound production. In: Busnel R-G, Fish JF, editors. Animal Sonar Systems. New York: Plenum Press. pp 239-249.
69. Ridgway SH, Carder DA. 1988. Nasal pressure and sound production in an echolocating white whale, Delphinapterus leucas. In: Nachtigall PE, Moore PWB, editors. Animal Sonar: Processes and Performance. New York: Plenum Press. pp 53-60.
70. Ridgway SH, Carder DA. 1990. Tactile sensitivity, somatosensory responses, skin vibrations, and the skin surface ridges of the bottlenose dolphin, Tursiops truncatus. In: Thomas J, Kastelein R, editors. Sensory Abilities of Cetaceans. New York: Plenum Press. pp 163-179.
71. Romeis B. 1989. Mikroskopische Technik. Munchen, Wien, Baltimore: Urban & Schwarzenberg.
72. Schenkkan EJ. 1973. On the comparative anatomy and function of the nasal tract in Odontocetes (Mammalia. Cetacea). Bijdragen tot de Dierkunde 43:127-159.
73. Schevill WE, Lawrence B. 1956. Food-Finding by a captive porpoise (Tursiops truncatus). Breviora 53:1-15.
74. Schwerdfeger WK, Oelschlager HA, Stephan H. 1984. Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei. Anat Embryol 170:11-19.
75. Slijper EJ. 1962. Whales. London: Hutchinson. 475 p.
76. Sokolov W. 1960. Some similarities and dissimilarities in the structure of the skin among the members of the suborders odontoceti and mystacoceti (cetacea). Nature 185:745-747.
77. Sokolov W. 1962. Adaptations of the mammalian skin to the aquatic mode of life. Nature 195:464-466.
78. Sokolov V, Kalashnikova M. 1971. The Ultrastructure of Epidermal Cells in Phocoena phocoena. In: Pilleri G, editor. Investigations on Cetacea 3. Benteli: Bern. pp 194-199.
79. Sokolov VE, Kalashnikova M, Rodionov V. 1973. Microand Ultrastructure of the skin in the harbour porpoise (Phocoena phocoena). In: Chapskii KK, Sokolov VE, editors. Morphology and Ecology in Marine Mammals. Chichester: Wiley. pp 82-101.
80. Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN. 2007. Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450:1190-1195.
81. Villadsgaard A, Wahlberg M, Tougaard J. 2007. Echolocation signals of wild harbour porpoises, Phocoena phocoena. J Exp Biol 210:56-64.
82. Von Baer KE. 1826. Die Nase der Cetaceen erlautert durch Untersuchung der Nase des Braunfisches (Delphinus phocaena). Isis von Oken 7-12:811-847.