Precocious Ossification of the Tympanoperiotic Bone in Fetal and Newborn Dolphins: An Evolutionary Adaptation to the Aquatic Environment?

Anatomical Record

Volumn 298, Issue 7, 2015, Pages 1294-1300

  Cozzi, Bruno ^a   Podestà, Michela ^b   Vaccaro, Calogero ^a   Poggi, Roberto ^c   Mazzariol, Sandro ^a   Huggenberger, Stefan ^d   Zotti, Alessandro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b Museum of Natural History of Milan   (Italy)

^c G Doria Civic Museum of Natural History   (Italy)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Dolphins; DXA; Fetal development; Tympanic bulla; Tympanoperiotic bone

Indexed keywords

AQUATIC ENVIRONMENT; ARTICLE; BONE DENSITY; BONE MATURATION; BOTTLENOSE DOLPHIN; COMMON DOLPHIN; DUAL ENERGY X RAY ABSORPTIOMETRY; EVOLUTIONARY ADAPTATION; FEMALE; MALE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; SKELETON; SKULL; STENELLA; TURSIOPS TRUNCATUS; X RAY BONE DENSITOMETER; ADAPTATION; ANIMAL; BONE DEVELOPMENT; DOLPHIN; ECOSYSTEM; EVOLUTION; NEWBORN; PHYSIOLOGY; TEMPORAL BONE;

BALAENOPTERA PHYSALUS; CETACEA; DELPHINUS DELPHIS; MAMMALIA; STENELLA (CETACEA); TURSIOPS TRUNCATUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL EVOLUTION; DOLPHINS; ECOSYSTEM; OSTEOGENESIS; TEMPORAL BONE;

EID: 84931577863     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.23120     Document Type: Article

References (36)

1. Ammann P, Rizzoli R, Slosman D, Bonjour JP. 1992. Sequential and precise in vivo measurement of bone mineral density in rats using dual-energy X-ray absorptiometry. J Bone Miner Res 7:311-316.
2. Carstanjen B, Duboeuf F, Detilleux J, Lepage OM. 2003. Equine third metacarpal bone assessment by quantitative ultrasound and dual energy X-ray absorptiometry: an ex vivo study. J Vet Med a Physiol Pathol Clin Med 50:42-47.
3. Cozzi B, Mazzariol S, Podestá M, Zotti A. 2009. Diving adaptations of the cetacean skeleton. Open Zool J 2:24-32.
4. Cozzi B, Panin M, Butti C, Podestà M, Zotti A. 2010. Bone density distribution patterns in the rostrum of delphinids and beaked whales: evidence of family-specific evolutive traits. Anat Rec 293:235-242.
5. Cozzi B, Podestà M, Mazzariol S, Zotti A. 2012. Fetal and early post-natal mineralization of the tympanic bulla in fin whales may reveal a hitherto undiscovered evolutionary trait. PloS One 7:e37110.
6. Cranford TW, Krysl P, Amundin M. 2010. A new acoustic portal into the odontocete ear and vibrational analysis of the tympanoperiotic complex. PLoS One 5:e11927.
7. Currey JD. 1979. Mechanical properties of bone tissues with greatly differing functions. J Biomechs 12:313-319.
8. de Buffrénil V, Dabin W, Zylrberg L. 2004. Histology and growth of the cetacean petro-tympanic bone complex. J Zool (Lond) 262:371-381.
9. De Muizon C. 2009. L'origine et l'histoire évolutive des cétacés. Comptes Rendus Palevol 8:295-309.
10. Felts WJL, Spurrell FA. 1965. Structural orientation and density in cetacean humeri. Am J Anat 116:171-203.
11. Felts WJL, Spurrell FA. 1966. Some structural and developmental characteristics of cetacean (odontocete) radii. A study of adaptive osteogenesis. Am J Anat 118:103-134.
12. Forbes HO. 1893. Observations on the development of the rostrum in the cetacean genus mesoplodon, with remarks on some of the species. Proc Zool Soc Lond 1893:216-236.
13. Gray N-M, Kainec K, Madar S, Tomko L, Wolfe S. 2007. Sink or swim? Bone density as a mechanism for buoyancy control in early cetaceans. Anat Rec 290:638-653.
14. Haddad D, Huggenberger S, Haas-Rioth M, Kossatz LS, Oelschläger HHA, Haase A. 2012. Magnetic resonance microscopy of prenatal dolphins (mammalia, odontoceti, delphinidae)-ontogenetic and phylogenetic implications. Zool Anz 251:115-130.
15. ISCD, International Society for Clinical densitometry. 2013. Official positions-adult and pediatric. The international society for clinical densitometry-official positions 2013, Middletown (CT), USA. Available at: www.ISCD.org
16. Kasuya T. 1973. Systematic consideration of recent toothed whales based on the morphology of the tympano-periotic bone. Sci Rep Whale Res Inst 25:1-103.
17. Lancaster WC, Ary WJ, Krysl P, Cranford TW. 2014. Precocial development within the tympanoperiotic complex in cetaceans. Mar Mammal Sci 31:369-375.
18. Mead JG, Fordyce RE. 2009. The Therian skull: a lexicon with emphasis on the odontocetes. Smithson Contrib Zool 627:1-216.
19. Miller GS. 1923. The telescoping of the cetacean skull. Washington, DC: Smithsonian Institution Publication 2720. p 1-70.
20. Moran MM, Nummela S, Thewissen JGM. 2011. Development of the skull of the pantropical spotted dolphin (Stenella attenuata). Anat Rec 294:1743-1756.
21. Nummela S. 2009. Hearing. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals, 2nd ed. San Diego, CA: Academic Press. p 553-562.
22. Nummela S, Thewissen JGM, Bajpai S, Hussain T, Kumar K. 2007. Sound transmission in archaic and modern whales: anatomical adaptations for underwater hearing. Anat Rec 290:716-733.
23. Oelschläger HA. 1990. Evolutionary morphology and acoustics in the dolphin skull. In: Thomas JA, Kastelein RA, editors. Sensory abilities of cetaceans. New York: Plenum Press. p 137-162.
24. Oelschläger HA, Buhl EH. 1985. Occurrence of an olfactory-bulb in the early development of the harbor porpoise (Phocoena phocoena L.). Fortschr Zool 30:695-698.
25. Pilleri G, Gihr M, Kraus C. 1989. The organ of hearing in cetacea. II. Paleobiological evolution. Investig Cetacea 22:5-185.
26. Price SA, Bininda-Emonds ORP, Gittleman JL. 2005. A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (cetartiodactyla). Biol Rev Camb Philos Soc 80:445-473.
27. Rauschmann MA, Huggenberger S, Kossatz LS, Oelschläger HHA. 2006. Head morphology in perinatal dolphins: a window into phylogeny and ontogeny. J Morphol 267:1295-1315.
28. Reidenberg JS, Laitman JT. 2008. Sisters of the sinuses: cetacean air sacs. Anat Rec 291:1389-1396.
29. Rommel SA. 2002. Skull anatomy. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals, 1st ed. San Diego, CA: Academic Press. p 1103-1117.
30. Rommel SA, Reynolds JE, III. 2002. Skeletal anatomy. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals, 1st ed. San Diego, CA: Academic Press. p 1089-1103.
31. Štěrba O, Klima M, Schildger B. 2000. Embryology of dolphins-staging and ageing of embryos and fetuses of some cetaceans. Adv Anat Embryol Cell Biol 157:1-133.
32. Thewissen JGM, Cooper LN, George JC, Bajpai S. 2009. From land to water: the origin of whales, dolphins, and porpoises. Evol Edu Outreach 2:272-288.
33. Zioupos P, Currey JD, Casinos A, De Buffrenil V. 1997. Mechanical properties of the rostrum of the whale mesoplodon densirostris, a remarkably dense bony tissue. J Zool 241:725-737.
34. Zotti A, Gianesella M, Ceccato C, Morgante M. 2010. Physiological values and factors affecting the metacarpal bone density of healthy feedlot beef cattle as measured by dual-energy X-ray absorptiometry. J Anim Physiol Anim Nutr 94:615-622.
35. Zotti A, Poggi R, Cozzi B. 2009. Exceptional bone density DXA values of the rostrum of a deep-diving marine mammal: a new technical insight in the adaptation of bone to aquatic life. Skeletal Radiol 38:1123-1125.
36. Zylberberg L, Traub W, De Buffrenil V, Allizard F, Arad T, Weiner S. 1998. Rostrum of a toothed whale: ultrastructural study of a very dense bone. Bone 23:241-247.