Life history constrains biochemical development in the highly specialized odontocete echolocation system

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1649, 2008, Pages 2327-2334

  Koopman, Heather N ^a   Zahorodny, Zoey P ^a,b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Development; Dolphin; Ontogeny; Porpoise; Vertebrate life history

Indexed keywords

FAT; LIPID;

BIOACCUMULATION; BIOLOGICAL DEVELOPMENT; DOLPHIN; ECHOLOCATION; FAT RESERVE; LIFE HISTORY; LIPID; MATERNAL CARE; ONTOGENY; PORPOISE; SKULL; SPATIAL DISTRIBUTION; SPECIALIZATION; WHALE;

ARTICLE; BIOCHEMISTRY; BOTTLENOSE DOLPHIN; ECHOLOCATION; INDEPENDENCE; LIPID STORAGE; MATERNAL CARE; NONHUMAN; ODONTOCETE; ONTOGENY; PORPOISE; PRIORITY JOURNAL; SOFT TISSUE; WHALE;

MAMMALIA; ODONTOCETI; PHOCOENIDAE; TURSIOPS; VERTEBRATA;

EID: 51449090348     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0457     Document Type: Article

References (65)

1. Albon, S. D., Clutton-Brock, T. H. & Guiness, F. E. 1987 Early development and population dynamics in red deer. II: density-independent effects and cohort variation. J. Anim. Ecol. 56, 69-81. (doi:10.2307/4800)
2. Brill, R. L. & Harder, P. J. 1991 The effects of attenuating returning echolocation signals at the lower jaw of a dolphin (Tursiops truncatus). J. Acoust. Soc. Am. 89, 2851-2857. (doi:10.1121/1.400723)
3. Burns, J. M., Costa, D. P., Frost, K. & Harvey, J. T. 2005 Development of body oxygen stores in harbor seals: effects of age, mass, and body composition. Phys. Biochem. Zool. 78, 1057-1068. (doi:10.1086/432922)
4. Cranford, T. W., Amundin, M. & Norris, K. S. 1996 Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J. Morphol. 228, 223-285. (doi:10.1002/(SICI)1097- 4687(199606)228:3〈223::AID-JMOR1〉3.0.CO;2-3)
5. Fordyce, R. E. 2002 Cetacean evolution. In Encyclopedia of marine mammals (eds W. F. Perrin, B. Würsig & J. G. M. Thewissen), pp. 214-220. San Diego, CA: Academic Press.
6. Fowler, S. L., Costa, D. P., Arnould, J. P. Y., Gales, N. J. & Burns, J. M. 2007 Ontogeny of oxygen stores and physiological diving capability in Australian sea lions. Funct. Ecol. 21, 922-935. (doi:10.1111/j.1365-2435.2007.01295.x)
7. Gardner, S. C. & Varanasi, U. 2003 Isovaleric acid accumulation in melon during development. Naturwissenschaften 90, 528-531. (doi:10.1007/s00114-003-0472-x)
8. Garton, G. A. & Duncan, W. R. H. 1969 Effect of diet and rumen development on the composition of adipose tissue triglycerides of the calf. Br. J. Nutr. 23, 421. (doi:10.1079/BJN19690049)
9. Garton, G. A. & Duncan, W. R. H. 2002 Composition of adipose tissue triglycerides of neonatal and year-old lambs. J. Sci. Food Agric. 20, 39-42. (doi:10.1002/jsfa.2740200110)
10. Geraci, J. R. & Lounsbury, V. J. 1993 Marine mammals ashore: a field guide for strandings. Galveston, TX: Texas A&M Sea Grant Publication.
11. Gouw, I. T. H. & Vlugter, J. C. 1967 Physical properties of triglycerides III: ultrasonic sound velocity. Fette Seif. Anstrich. 69, 159-164. (doi:10.1002/lipi.19670690301)
12. Hanken, J. & Gross, J. B. 2005 Evolution of cranial development and the role of neural crest: insights from amphibians. J. Anat. 207, 437-446.
13. Hanken, J. & Hall, B. K. (eds) 1993 The skull, vol. 3. Chicago, IL: University of Chicago Press.
14. Helms, J. A., Cordero, D. & Tapadia, M. D. 2005 New insights into craniofacial morphogenesis. Development 132, 851-861. (doi:10.1242/dev.01705)
15. Hustad, G. O., Richardson, T., Winder, W. C. & Dean, M. P. 1971 Acoustic properties of some lipids. Chem. Phys. Lipids 7, 61-74. (doi:10.1016/0009-3084(71)90020-X)
16. Iverson, S. J. 1993 Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symp. Zool. Soc. Lond. 66, 263-291.
17. Iverson, S. J. & Oftedal, O. T. 1995 Phylogenetic and ecological variation in the fatty acid composition of milks. In Handbook of milk composition (ed. R. G. Jensen), pp. 789-827. San Diego, CA: Academic Press.
18. Kadim, I. T., Mahgoub, O., Al-Maqbaly, R. S., Annamalai, K. & Al-Ajmi, D. S. 2002 Effects of age on fatty acid composition of the hump and abdomen depot fats of the Arabian camel (Camelus dromedarius). Meat Sci. 62, 245-251. (doi:10.1016/S0309-1740(01)00254-6)
19. Kastelein, R. A. & van Battum, R. 1990 The relationship between body weight and morphological measurements in harbour porpoises (Phocoena phocoena) from the North Sea. Aquat. Mamm. 16, 48-52.
20. Koopman, H. N. 2007 Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes. Mar. Biol. 151, 277-291. (doi:10.1007/s00227-006-0489-8)
21. Koopman, H. N., Pabst, D. A., McLellan, W. A., Dillaman, R. M. & Read, A. J. 2002 Changes in blubber distribution and morphology associated with starvation in the harbour porpoise (Phocoena phocoena): evidence for regional differences in blubber structure and function. Phys. Biochem. Zool. 75, 498-512. (doi:10.1086/342799)
22. Koopman, H. N., Iverson, S. J. & Read, A. J. 2003 High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon. J. Comp. Phys. B 173, 247-261.
23. Koopman, H. N., Budge, S. M., Ketten, D. R. & Iverson, S. J. 2006 Topographical distribution of lipids inside the mandibular fat bodies of odontocetes: remarkable complexity and consistency. IEEE J. Oceanic Eng. 31, 95-106. (doi:10.1109/JOE.2006.872205)
24. Kuczaj, S. A. 2004 The ontogeny of the dolphin echolocation system. Final Report to the U.S. Office of Naval Research for Grant N00014-00-1-0427, University of Southern Mississippi.
25. Kuritani, S., Matsuo, I. & Aizawa, S. 1997 Developmental patterning and evolution of the mammalian viscerocranium: genetic insights into comparative morphology. Dev. Dyn. 209, 139-155. (doi:10.1002/(SICI)1097- 0177(199706)209:2〈139::AID-AJA1〉3.0.CO;2-J)
26. Li, S., Wang, D., Wang, K., Xiao, J. & Akamatsu, T. 2007 The ontogeny of echolocation in a Yangtze finless porpoise (Neophocoena phocaenoides asiaeorientalis) (L). J. Acoust. Soc. Am. 122, 715-718. (doi:10.1121/1.2747203)
27. Litchfield, C., Karol, R. & Greenberg, A. 1973 Compositional topography of melon lipids in the Atlantic bottlenosed dolphin Tursiops truncatus: implications for echo-location. Mar. Biol. 23, 165-169. (doi:10.1007/BF00389480)
28. Litchfield, C., Greenberg, A. J., Caldwell, D. K., Caldwell, M. C., Sipos, J. C. & Ackman, R. G. 1975 Comparative lipid patterns in acoustical and nonacoustical fatty tissues of dolphins, porpoises and toothed whales. Comp. Biochem. Physiol. B 50, 591-597. (doi:10.1016/0305-0491(75) 90095-4)
29. Lodge, G. A., Sarkar, N. K. & Kramer, J. G. K. 1978 Fat deposition and fatty acid composition in the neonatal pig. J. Anim. Sci. 47, 497-504.
30. Madsen, P. T., Carder, D. A., Au, W. W. L., Nachtigall, P. E., Møhl, B. & Ridgway, S. H. 2003 Sound production in neonate sperm whales. J. Acoust. Soc. Am. 113, 2988-2991. (doi:10.1121/1. 1572137)
31. Malins, D. C. & Varanasi, U. 1975 Cetacean biosonar, Part II: the biochemistry of lipids in acoustic tissues. In Biochemical and biophysical perspectives in marine biology, vol. 2 (eds D. C. Malins & J. R. Sargent), pp. 237-290. London, UK: Academic Press.
32. Maxia, C., Scano, P., Maggiani, F., Murtas, D., Piras, F., Crnjar, R., Lai, A. & Sirigu, P. 2007 A morphological and 13C NMR study of the extramandibular fat bodies of the striped dolphin (Stenella coeruleoalba). Anat. Rec. 290, 913-919. (doi:10.1002/ar.20560)
33. McLellan, W. A., Koopman, H. N., Rommel, S. A., Read, A. J., Potter, C. W., Nicolas, J. R., Westgate, A. J. & Pabst, D. A. 2002 Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena L.) from the western north Atlantic. J. Zool. Lond. 257, 457-472. (doi:10.1017/S0952836902001061)
34. Mead, J. F., Alfin-Slater, R. B., Howton, D. R. & Popják, G. 1986 Lipids: chemistry, biochemistry and nutrition. New York, NY: Plenum Press.
35. Møhl, B., Au, W. W. L., Pawloski, J. & Nachtigall, P. E. 1999 Dolphin hearing: relative sensitivity as a function of point of application of a contact sound source in the jaw and head region. J. Acoust. Soc. Am. 105, 3421-3424. (doi:10.1121/1.426959)
36. Moore, W. J. 1981 The mammalian skull. New York, NY: Cambridge University Press.
37. Morii, H. & Kaneda, T. 1982 Biosynthesis of branched-chain fatty acids from branched-chain amino acids in subcutaneous tissue of the marine little toothed whale, Stenella caeruleo-alba. Comp. Biochem. Physiol. B 71, 357-365. (doi:10.1016/0305-0491(82)90395-9)
38. Morris, R. J. 1975 Further studies into the lipid structure of the spermaceti organ of the sperm whale (Physeter catodon). Deep-Sea Res. 22, 483-489.
39. Morris, R. J. 1986 The acoustic faculty of dolphins. In Research on dolphins (eds M. M. Bryden & R. Harrison), pp. 369-399. Oxford, UK: Clarendon Press.
40. Nachtigall, P. E., Yuen, M. L., Mooney, T. A. & Taylor, K. A. 2005 Hearing measurements from a stranded infant Risso's dolphin, Grampus griseus. J. Exp. Biol. 208, 4181-4188. (doi:10.1242/jeb.01876)
41. Noren, S. R., Williams, T. M., Pabst, D. A., McLellan, W. A. & Dearolf, J. L. 2001 The development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins and seals for activity during submergence. J. Comp. Phys. B 171, 127-134. (doi:10.1007/ s003600000161)
42. Norris, K. S. 1968 The evolution of acoustic mechanisms in odontocete cetaceans. In Evolution and environment (ed. E. T. Drake), pp. 297-324. New Haven, CT: Yale University Press.
43. Olsson, L., Ericsson, R. & Cerny, R. 2005 Vertebrate head development: segmentation, novelties, and homology. Theory Biosci. 124, 145-163.
44. Pond, C. M. 1984 Physiological and ecological importance of energy storage in the evolution of lactation: evidence for a common pattern of anatomical organization of adipose tissue in mammals. Symp. Zool. Soc. Lond. 51, 1-32.
45. Pond, C. M. 1998 The fats of life. Cambridge, UK: Cambridge University Press.
46. Pond, C. M., Mattacks, C. A., Colby, R. H. & Ramsay, M. A. 1992 The anatomy, chemical composition, and metabolism of adipose tissue in wild polar bears (Ursus maritimus). Can. J. Zool. 70, 326-341.
47. Ramsay, M. A. & Dunbrack, R. L. 1986 Physiological constraints on life history phenomena: the example of small bear cubs at birth. Am. Nat. 127, 735-743. (doi:10.1086/284522)
48. Razak, K. A. & Fusessery, Z. M. 2007 Development of functional organization of the pallid bat auditory cortex. Hear. Res. 228, 69-81. (doi:10.1016/j.heares.2007.01.020)
49. Read, A. J. 1999 Harbour porpoise Phocoena phocoena (Linnaeus, 1758). In Handbook of marine mammals: the second book of dolphins and porpoises, vol. 6 (eds S. H. Ridgway & R. Harrison), pp. 323-355. San Diego, CA: Academic Press.
50. Read, A. J. & Hohn, A. A. 1995 Life in the fast lane: the life history of harbor porpoises from the Gulf of Maine. Mar. Mamm. Sci. 11, 423-440. (doi:10.1111/j.1748-7692.1995.tb00667.x)
51. Ridgway, S. H. & Carder, D. A. 1997 Hearing deficits measured in some Tursiops truncatus, and the discovery of a deaf/mute dolphin. J. Acoust. Soc. Am. 101, 590-594. (doi:10.1121/1.418122)
52. Scano, P., Maxia, C., Maggiani, F., Crnjar, R., Lai, A. & Sirigu, P. 2005 Histological and NMR study of the melon of the striped dolphin (Stenella coeruleoalba). Chem. Phys. Lipids 134, 21-28. (doi:10.1016/j. chemphyslip.2004.10.001)
53. Seilacher, A. 1970 Arbeitskonzept zur Konstruktions-Morphologie. Lethaia 3, 393-396. (doi:10.1111/j.1502-3931.1970.tb00830.x)
54. Smith, R. J. & Read, A. J. 1992 Consumption of euphausiids by harbour porpoise (Phocoena phocoena) calves in the Bay of Fundy. Can. J. Zool. 70, 1629-1632.
55. Steel, R. G. D. & Torrie, J. H. 1980 Principles and procedures of statistics: a biometrical approach. New York, NY: McGraw-Hill Book Company.
56. Tanaka, K., Budd, M. A., Efron, M. L. & Isselbacher, K. J. 1966 Isovaleric acidemia: a new genetic defect of leucine metabolism. Proc. Natl Acad. Sci. USA 56, 236-242. (doi:10.1073/pnas.56.1.236)
57. Thomson, K. S. 1988 Morphogenesis and evolution. New York, NY: Oxford University Press.
58. Trainor, P. 2003 The bills of ducks and quails. Science 299, 523-524. (doi:10.1126/science.1081521)
59. Tranel, K. & Kuczaj, S. 2005 Ontogeny of echolocation in bottlenose dolphins (Tursiops truncatus) during the first six months of life. In Abstracts of the Sixteenth Biennial Conference on the Biology of Marine Mammals, San Diego, CA, p. 283.
60. Varanasi, U., Feldman, H. R. & Malins, D. C. 1975 Molecular basis for formation of lipid sound lens in echolocating cetaceans. Nature 255, 340-343. (doi:10.1038/255340a0)
61. Varanasi, U., Markey, D. & Malins, D. C. 1982 Role of isovaleroyl lipids in channelling of sound in the porpoise melon. Chem. Phys. Lipids 31, 237-244. (doi:10.1016/0009-3084(82)90059-7)
62. Wells, R. S. 2003 Dolphin social complexity: lessons from long-term study and life-history. In Animal social complexity: intelligence, culture, and individualized societies (eds F. B. M. de Waal & P. L. Tyack), pp. 32-56. Cambridge, MA: Harvard University Press.
63. Wells, R. S. & Scott, M. D. 1999 Bottlenose dolphin Tursiops truncatus (Montagu, 1821). In Handbook of marine mammals: the second book of dolphins and porpoises, vol. 6 (eds S. H. Ridgway & R. Harrison), pp. 137-182. San Diego, CA: Academic Press.
64. Wretlind, A. 1957 The toxicity of low-molecular triglycerides. Acta. Physiol. Scand. 40, 338-343.
65. Zelditch, M. 2003 Space, time and repatterning. In Keywords and concepts in evolutionary developmental biology (eds B. K. Hall & W. M. Olson), pp. 341-349. Cambridge, MA: Harvard University Press.