Lactation in Whales and Dolphins: Evidence of Divergence Between Baleen- and Toothed-Species

Article

Abstract

Although it has been more than one hundred years since the first publication on the milks of whales and dolphins (Order Cetacea), information on lactation in these species is scattered and fragmentary. Yet the immense size of some cetaceans, and the recent evidence that another group of marine mammals, the true seals, have remarkable rates of secretion of milk fat and energy, make this group of great comparative interest. In this paper information on lactation patterns, milk composition and lactation performance is reviewed. Two very different patterns are evident. Many of the baleen whales (Suborder Mysticeti) have relatively brief lactations (5–7 months) during which they fast or eat relatively little. At mid-lactation they produce milks relatively low in water (40–53%), high in fat (30–50%), and moderately high in protein (9–15%) and ash (1.2–2.1%). From mammary gland weights and postnatal growth rates, it is predicted that their energy outputs in milk are exceptional, reaching on the order of 4000 MJ/d in the blue whale. This is possible because pregnant females migrate to feeding grounds where they can ingest and deposit great amounts of energy, building up blubber stores prior to parturition. On the other hand, the toothed whales and dolphins (Suborder Odontoceti) have much more extensive lactations typically lasting 1–3 years, during which the mothers feed. At mid-lactation their milks appear to be higher in water (60–77%) and lower in fat (10–30%) and ash (0.6–1.1%), with similar levels of protein (8–11%). At least some odontocetes resemble primates in terms of low predicted rates of energy output and a long period of dependency of the young. However, these hypotheses are based on small numbers of samples for a relatively small number of species. Much of the available data on milk composition is of rather poor quality; for example, it is not possible to determine if milk composition changes over the course of lactation among odontocetes. Additional research on cetacean mammary glands and their secretions is needed to understand the reproductive strategies of these fascinating animals.

Whales dolphins marine mammals lactation duration milk composition milk yield 

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REFERENCES

  1. 1.
    O. T. Oftedal, W. D. Bowen, and D. J. Boness (1993). Energy transfer by lactating hooded seals, and nutrient deposition in their pups, during the four days from birth to weaning. Physiol. Zool. 66:412–435.Google Scholar
  2. 2.
    O. T. Oftedal (1993). The adaptation of milk secretion to the constraints of fasting in bears, seals and baleen whales. J. Dairy Sci. 76:3234–3246.Google Scholar
  3. 3.
    S. J. Iverson, O. T. Oftedal, W. D. Bowen, D. J. Boness, and J. Sampugna (1995). Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal. J. Comp. Physiol. 165B:1–12.Google Scholar
  4. 4.
    S. J. Iverson, W. D. Bowen, D. J. Boness, and O. T. Oftedal (1993). The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol. Zool. 66:61–88.Google Scholar
  5. 5.
    M. B. Kretzmann, D. P. Costa, and B. J. LeBoeuf (1993). Maternal energy investment in elephant seal pups: evidence for sexual equality? Am. Natl. 141:466–480.Google Scholar
  6. 6.
    C. Lydersen, M. O. Hammill, and K. M. Kovacs (1995). Milk intake, growth and energy consumption in pups of ice-breeding grey seals (Halichoerus grypus) from the Gulf of St. Lawrence, Canada. J. Comp. Physiol. 164B:585–592.Google Scholar
  7. 7.
    O. T. Oftedal, W. D. Bowen, and D. J. Boness (1996). Lactation performance and nutrient deposition in pups of the harp seal, Phoca groenlandica, on ice floes off southeast Labrador. Physiol. Zool. 69:635–657.Google Scholar
  8. 8.
    O. T. Oftedal (1984). Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. Lond. 51:33–85.Google Scholar
  9. 9.
    E. J. Slijper (1962). Whales, Hutchinson and Co., London.Google Scholar
  10. 10.
    O. T. Oftedal (1980). Milk composition and formula selection for hand-rearing young mammals. In E. R. Maschgan, M. E. Allen, and L. E. Fisher (eds.), Dr. Scholl Nutrition Conference—A conference on the Nutrition of Captive Wild Animals, Lincoln Park Zoological Gardens, Chicago, Illinois, pp. 67–83.Google Scholar
  11. 11.
    P. Purdie (1885). Chemical composition of the milk of the porpoise. Chem. News J. Phys. Sci. 52:170.Google Scholar
  12. 12.
    O. T. Oftedal and S. J. Iverson (1987). Hydrogen isotope methodology for the measurement of milk intake and the energetics of growth in suckling young. In A. C. Huntley, D. P. Costa, G. A. J. Worthy, and M. A. Castellini (eds.), Approaches to Marine Mammal Energetics, Society for Marine Mammalogy, pp. 67–96.Google Scholar
  13. 13.
    D. P. Costa (1991). Reproductive and foraging energetics of pinnipeds: implications for life history patterns. In D. Renouf (ed.), Behaviour of Pinnipeds, Chapman and Hall, London, pp. 300–344.Google Scholar
  14. 14.
    D. J. Boness and W. D. Bowen (1996). The evolution of maternal care in pinnipeds. Bioscience 46:645–654.Google Scholar
  15. 15.
    O. T. Oftedal, D. J. Boness, and R. A. Tedman (1987). The behavior, physiology, and anatomy of lactation in the Pinnipedia. Curr. Mammal. 1:175–245.Google Scholar
  16. 16.
    W. Scoresby (1820). An Account of the Arctic Regions with a History and a Description of the Northern Whale-Fishery, Archibald Constable, Edinburgh, Scotland.Google Scholar
  17. 17.
    F. D. Bennett (1840). Narrative of a Whaling Voyage Round the Globe from the Year 1833 to 1836, Richard Bentley, London.Google Scholar
  18. 18.
    C. M. Scammon (1874). The Marine Mammals of the Northwestern Coast of North America, Described and illustrated, together with an account of the American Whale-Fishery, John H. Carmany, San Francisco.Google Scholar
  19. 19.
    D. G. Lillie (1915). Cetacea. In British Antarctic (“Terra Nova”) Expedition, 1910. Natural History Report. Zoology, British Museum (Natural History), London, pp. 85–124.Google Scholar
  20. 20.
    M. Takata (1922). Untersuchungen über Cetacea. II. Über die Milch des Finnwals. Tohuku J. Exper. Med. 2:344–354.Google Scholar
  21. 21.
    K. Takemura (1927). Untersuchungen über Cetacea. XXVII. Über die Milch verschiedener Walarten. Jap. J. Med. Sci. II. Biochem. 1:131–134.Google Scholar
  22. 22.
    N. A. Mackintosh and J. F. G. Wheeler (1929). Southern blue and fin whales. Discov. Rep. 1:257–540.Google Scholar
  23. 23.
    Tönnesen and Johnsen (1982). The History of Modern Whaling. University of California Press, Berkeley, Caifornia.Google Scholar
  24. 24.
    E. W. van Lennep and E. W. van Utrecht (1953). Preliminary report on the study of the mammary glands of whales. Norsk Hvalfangst-Tid. 42:249–258.Google Scholar
  25. 25.
    R. G. Chittleborough (1958). The breeding cycle of the female humpback whale Megaptera nodosa. Austr. J. Mar. Freshw. Res. 9:1–18.Google Scholar
  26. 26.
    D. E. Sergeant (1962). The biology of the pilot or pothead whale Globicephala malaena(Traill) in Newfoundland waters. Bull. Fish. Res. Bd. Can. 132:1–84.Google Scholar
  27. 27.
    P. B. Best, P. A. S. Canham, and N. Macleod (1984). Patterns of reproduction in sperm whales, Physeter macrocephalus. Rep. Int. Whal. Commn.(Special issue) 6:51–79.Google Scholar
  28. 28.
    S. H. Shane, R. S. Wells, and B. Wursig (1986). Ecology, behavior and social organization of the bottlenose dolphin: a review. Mar. Mammal Sci. 2:34–63.Google Scholar
  29. 29.
    W. F. Perrin and S. B. Reilly (1984). Reproductive parameters of dolphins and small whales of the family Delphinidae. Rep. Int. Whal. Commn.(Special issue) 6:97–133.Google Scholar
  30. 30.
    W. D. Bowen (1991). Behavioural ecology of pinniped neonates. In D. Renouf (ed.), Behaviour of Pinnipeds, Chapman and Hall, London, pp. 66–127.Google Scholar
  31. 31.
    C. Lockyer (1981). Growth and energy budgets of large baleen whales from the southern hemisphere. In Mammals in the Seas. FAO Fisheries Series No. 5, Vol. 3, Food and Agriculture Organization of the United Nations, Rome, Italy, pp. 379–487.Google Scholar
  32. 32.
    C. Lockyer (1984). Review of baleen whale (Mysticeti) reproduction and implications for management. Rep. Int. Whal. Commn.(Special issue) 6:27–50.Google Scholar
  33. 33.
    P. B. Best (1966). A case of prolonged lactation in the fin whale (Balaenoptera physalus). Norsk Hvalfangst-Tid. 55:119–122.Google Scholar
  34. 34.
    C. Lockyer (1981). Estimation of the energy costs of growth, maintenance and reproduction in the female minke whale, (Balaenoptera acutorostrata), from the southern hemisphere. Rep. Int. Whal. Commn. 31:337–343.Google Scholar
  35. 35.
    P. B. Best (1982). Seasonal abundance, feeding, reproduction, age and growth in minke whales off Durban (with incidental observations from the Antarctic). Rep. Int. Whal. Commn. 32:759–786.Google Scholar
  36. 36.
    R. G. Chittleborough (1965). Dynamics of two populations of the humpback whale, Megaptera novaeangliae(Borowski). Aust. J. Mar. Freshw. Res. 16:33–128.Google Scholar
  37. 37.
    D. A. Glockner-Ferrari and M. J. Ferrari (1984). Reproduction in humpback whales, Megaptera novaeangliae, in Hawaiian waters. Rep. Int. Whal. Commn. 6:237–242.Google Scholar
  38. 38.
    L. Baraff and M. T. Weinrich (1993). Separation of humpback whale mothers and calves on a feeding ground in early autumn. Mar. Mammal Sci. 9:431–434.Google Scholar
  39. 39.
    S. L. Swartz (1986). Gray whale migratory, social and breeding behavior. Rep. Int. Whal. Commn.(Special issue) 8:207–229.Google Scholar
  40. 40.
    D. W. Rice and A. A. Wolman (1971). The Life History and Ecology of the Gray Whale (Eschrichtius robustus). Special Publication No. 3, American Society of Mammalogists, Stillwater, Oklahoma.Google Scholar
  41. 41.
    W. R. Koski, R. A. Davis, G. W. Miller, and D. E. Withrow (1993). Reproduction. In J. J. Burns, J. J. Montague, and C. J. Cowles (eds.), The Bowhead Whale, Society for Marine Mammalogy, Spec. Publication 2, Lawrence, Kansas, pp. 239–274.Google Scholar
  42. 42.
    L. F. Lowry (1993). Foods and feeding ecology. In J. J. Burns, J. J. Montague, and C. J. Cowles (eds.), The Bowhead Whale, Society for Marine Mammalogy, Lawrence, Kansas, pp. 201–238.Google Scholar
  43. 43.
    P. K. Hamilton, M. K. Marx, and S. D. Kraus (1995). Weaning in North Atlantic right whales. Mar. Mammal Sci. 11:386–390.Google Scholar
  44. 44.
    D. E. Gaskin (1982). The Ecology of Whales and Dolphins. Heinemann, London.Google Scholar
  45. 45.
    T. Kasuya (1985). Effect of exploitation on reproductive parameters of the spotted and striped dolphins off the Pacific coast of Japan. Sci. Rep. Whales Res. Inst. 36:107–138.Google Scholar
  46. 46.
    J. E. Heyning (1988). Presence of solid food in a young calf killer whale (Orcinus orca). Mar. Mammal Sci. 4:68–71.Google Scholar
  47. 47.
    N. J. Haenel (1986). General notes on the behavioral ontogeny of Puget Sound killer whales and the occurrence of allomaternal behavior. In B. C. Kirkevold and J. S. Lockard (eds.), Behavioral Biology of Killer Whales, Alan R. Liss, Inc., New York, pp. 285–300.Google Scholar
  48. 48.
    T. Kasuya and H. Marsh (1984). Life history and reproductive biology of the short-finned pilot whale, Globicephala macrorhynchus, off the Pacific coast of Japan. Rep. Int. Whal. Commn.(Special issue) 6:259–310.Google Scholar
  49. 49.
    S. Ridgway, T. Kamolnick, M. Reddy, and C. Curry (1995). Orphan-induced lactation in Tursiopsand analysis of collected milk. Mar. Mammal Sci. 11:172–182.Google Scholar
  50. 50.
    P. B. Best (1968). The sperm whale (Physeter catodon) off the west coast of South Africa. 2. Reproduction in the female. Investl. Rep. Div. Sea Fish. S. Afr. 66:1–32.Google Scholar
  51. 51.
    R. Gambell (1972). Sperm whales off Durban. Discov. Rep. 35:199–358.Google Scholar
  52. 52.
    A. J. Read and A. A. Hohn (1995). Life in the fast lane: the life history of harbor porpoises from the Gulf of Maine. Mar. Mammal Sci. 11:423–440.Google Scholar
  53. 53.
    D. E. Gaskin, G. J. D. Smith, A. P. Watson, W. Y. Yasui, and D. B. Yurick (1984). Reproduction in the porpoises (Phocoenidae): Implications for management. Rep. Int. Whal. Commn.(Special issue) 6:135–148.Google Scholar
  54. 54.
    R. L. Brownell (1984). Review of reproduction in platanistid dolphins. Rep. Int. Whal. Commn.(Special issue) 6:149–158.Google Scholar
  55. 55.
    J. G. Mead (1984). Survey of reproductive data for the beaked whales (Ziphiidae). Rep. Int. Whal. Commn.(Special issue) 6:91–96.Google Scholar
  56. 56.
    D. E. Sergeant (1973). Biology of white whales (Delphinapterus leucas) in western Hudson Bay. J. Fish. Res. Board Can. 30:1065–1090.Google Scholar
  57. 57.
    H. W. Braham (1984). Review of reproduction in the white whale, Delphinapterus leucas, narwhal, Monodon monoceros, and Irrawady dolphin, Orcaella brevirostris, with comments on stock assessment. Rep. Int. Whal. Commn.(Special Issue) 6:81–89.Google Scholar
  58. 58.
    W. N. Bonner (1984). Lactation strategies in pinnipeds: Problems for a marine mammalian group. Symp. Zool. Soc. Lond. 51:253–272.Google Scholar
  59. 59.
    W. D. Bowen, O. T. Oftedal, and D. J. Boness (1992). Mass and energy transfer during lactation in a small phocid, the harbor seal (Phoca vitulina). Physiol. Zool. 65:844–866.Google Scholar
  60. 60.
    D. J. Boness, W. D. Bowen, and O. T. Oftedal (1994). Evidence of a maternal foraging cycle resembling that of otariid seals in a small phocid, the harbor seal. Behav. Ecol. Sociobiol. 34:95–104.Google Scholar
  61. 61.
    B. P. Kelly and D. Wartzok (1996). Ringed seal diving behavior in the breeding season. Can. J. Zool. 74:1547–1555.Google Scholar
  62. 62.
    A. Scheibe (1908). Die Zusammensetzung der Walfischmilch. Münchener Med. Wochenschr. 55:795–796.Google Scholar
  63. 63.
    O. T. Oftedal and S. J. Iverson (1995). Phylogenetic variation in the gross composition of milks. In R. G. Jensen (ed.), Handbook of Milk Composition, Academic Press, New York, pp. 749–789.Google Scholar
  64. 64.
    A. A. Berzin (1972). The Sperm Whale(Kashalot). Israel Program for Scientific Translations, Jerusalem.Google Scholar
  65. 65.
    B. A. Zenkovich (1938). Milk of large-sized cetaceans. Comptes Rendus(Doklady) Acad. Sci. URSS 22:203–205.Google Scholar
  66. 66.
    C. Lockyer (1981). Estimates of growth and energy budget for the sperm whale Physeter catodon. In Mammals in the Seas. FAO Fisheries Series No. 5, Vol. 3, General Papers and Large Cetaceans, Food and Agriculture Organization, Rome, pp. 489–504.Google Scholar
  67. 67.
    A. V. Yablokov, V. M. Belkovich, and V. I. Borisov (1974). Whales and Dolphins. Part I. National Technical Information Service, Springfield, Virginia.Google Scholar
  68. 68.
    S. E. J. Daly, A. Di Rosso, R. A. Owens, and P. E. Hartmann (1993). Degree of breast emptying explains changes in the fat content, but not fatty acid composition of human milk. Exper. Physiol. 78:741–755.Google Scholar
  69. 69.
    O. T. Oftedal, D. J. Boness, and W. D. Bowen (1988). The composition of hooded seal (Cystophora cristata) milk: an adaptation for postnatal fattening. Can. J. Zool. 66:318–322.Google Scholar
  70. 70.
    J. P. Y. Arnould and I. L. Boyd (1995). Inter-and intra-annual variation in milk composition in Antarctic fur seals (Arctocephalus gazella). Physiol. Zool. 68:1164–1180.Google Scholar
  71. 71.
    J. C. D. White (1953). Composition of whales' milk. Nature 171:612.Google Scholar
  72. 72.
    M. E. Gregory, S. K. Kon, S. J. Rowland, and S. Y. Thompson (1955). The composition of the milk of the blue whale. J. Dairy Res. 22:108–112.Google Scholar
  73. 73.
    M. E. Q. Pilson and D. W. Waller (1970). Composition of milk from spotted and spinner porpoises. J. Mammal. 51:74–79.Google Scholar
  74. 74.
    R. Jenness and D. K. Odell (1978). Composition of milk of the pygmy sperm whale (Kogia breviceps). Comp. Biochem. Physiol. 61A:383–386.Google Scholar
  75. 75.
    M. M. Bryden (1968). Lactation and suckling in relation to early growth of the southern elephant seal. Aust. J. Zool. 16:739–747.Google Scholar
  76. 76.
    M. Peaker and J. A. Goode (1978). The milk of the fur seal, Arctocephalus tropicalis gazella;in particular the composition of the aqueous phase. J. Zool., London 185:469–476. [Correct species designation: Mirounga leonina]Google Scholar
  77. 77.
    A. R. Carlini, M. E. I. Marquez, G. Soave, D. F. Vergani, and P. A. Ronayne de Ferrer (1994). Southern elephant seal, Mirounga leonina:composition of milk during lactation. Polar Biol. 14:37–42.Google Scholar
  78. 78.
    M. A. Hindell, M. M. Bryden, and H. R. Burton (1994). Early growth and milk composition in southern elephant seals (Mirounga leonina). Aust. J. Zool. 42:723–732.Google Scholar
  79. 79.
    M. Riedman and C. L. Ortiz (1979). Changes in milk composition during lactation in the northern elephant seal. Physiol. Zool. 52:240–249.Google Scholar
  80. 80.
    M. B. Kretzmann, D. P. Costa, L. V. Higgins, and D. J. Needham (1991). Milk composition of Australian sea lions, Neophoca cinerea:variability in lipid content. Can. J. Zool. 69:2556–2561.Google Scholar
  81. 81.
    D. M. Ben Shaul (1962). The composition of the milk of wild animals. Int. Zoo Yearbk. 4:333–342.Google Scholar
  82. 82.
    R. Jenness and R. E. Sloan (1970). The composition of milks of various species: a review. Dairy Sci. Abstr. 32:599–612.Google Scholar
  83. 83.
    G. J. B. Ross (1984). Cetaceans of the south east coast of southern Africa. Ann. Cape Prov. Mus.(Nat. Hist.) 15:173–410.Google Scholar
  84. 84.
    V. M. Peddemors, H. J. H. de Muelenaere, and K. Devchand (1989). Comparative milk composition of the bottlenosed dolphin (Tursiops truncatus), humpback dolphin (Sousa plumbea) and common dolphin (Delphinus delphis) from southern African waters. Comp. Biochem. Physiol. A94:639–641.Google Scholar
  85. 85.
    G. J. B. Ross (1979). Records of pygmy and dwarf sperm whales, genus Kogia, from southern Africa, with biological notes and some comparisons. Ann. Cape Prov. Mus. (Nat. Hist.) 11:259–327.Google Scholar
  86. 86.
    S. Pervaiz and K. Brew (1986). Composition of the milks of the bottlenose dolphin (Tursiops truncatus) and the Florida manatee (Trichechus manatus latirostris). Comp. Biochem. Physiol. A84:357–360.Google Scholar
  87. 87.
    A. Klem (1935). Studies in the biochemistry of whale oils. Hvalraad. Skrifter 11:49–108.Google Scholar
  88. 88.
    S. J. Iverson and O. T. Oftedal (1995). Phylogenetic and ecological variation in the fatty acid composition of milks. In R. G. Jensen (ed.), Handbook of Milk Composition, Academic Press, New York, pp. 789–827.Google Scholar
  89. 89.
    R. G. Ackman, C. A. Eaton, and S. N. Hooper (1968). Lipids of the fin whale (Balaenoptera physalus) from North Atlantic waters. IV. Fin whale milk. Can. J. Biochem. 46:198–203.Google Scholar
  90. 90.
    R. G. Ackman, C. A. Eaton, and E. D. Mitchell (1971). The bottle-nosed dolphin Tursiops truncatus:Fatty acid composition of milk tryglyerides. Can. J. Biochem. 49:1172–1174.Google Scholar
  91. 91.
    J. S. Cama and M. L. Meara (1953). The component milk fats of Balaenoptera physalus(Finner whale). Biochem. J. 55:365–368.Google Scholar
  92. 92.
    B. H. Lauer and B. E. Baker (1969). Whale milk. I. Fin whale (Balaenoptera physalus) and beluga whale (Delphinapterus leucas) milk: gross composition and fatty acid constitution. Can. J. Zool. 47:95–97.Google Scholar
  93. 93.
    R. L. Glass and R. Jenness (1971). Comparative biochemical studies of milks—VI. Constituent fatty acids of milk fats of additional species. Comp. Biochem. Physiol. 38B:353–359.Google Scholar
  94. 94.
    H. Morii (1981). Fatty acids in milk of marine little toothed whales Stenella attenuata. Bull. Jap. Soc. Sci. Fish. 47:1367–1370.Google Scholar
  95. 95.
    S. J. Iverson, K. J. Frost, and L. F. Lowry (1997). Fatty acid signatures reveal fine scale structure of foraging distribution of harbour seals and their prey in Prince William Sound, Alaska. Marine Ecol. Progr. Ser.(in press).Google Scholar
  96. 96.
    M. Messer, E. A. Crisp, and K. Newgrain (1988). Studies on the carbohydrate content of milk of the crabeater seal (Lobodon carcinophagus). Comp. Biochem. Physiol. 90B:367–370.Google Scholar
  97. 97.
    D. E. Ullrey, C. C. Schwartz, P. A. Whetter, T. Rajeshwar Rao, J. R. Euber, S. G. Cheng, and J. R. Brunner (1984). Blue-green color and composition of Stejneger's beaked whale (Mesoplodon stejnegeri) milk. Comp. Biochem. Physiol. 79B:349–352.Google Scholar
  98. 98.
    C. A. Harms (1993). Composition of prepartum secretions of two bowhead whales (Balaena mysticetus L.). J. Wildl. Dis. 29:94–97.Google Scholar
  99. 99.
    S. Pervaiz and K. Brew (1986). Purification and characterization of the major whey proteins from the milks of the bottlenose dolphin (Tursiops truncatus), the Florida manatee (Trichechus manatus latirostris) and the beagle (Canis familiaris). Archives of Biochem. Biophysics 246:846–854.Google Scholar
  100. 100.
    F. W. Brambell (1970). The Transmission of Passive Immunity from Mother to Young, American Elsevier, New York.Google Scholar
  101. 101.
    M. E. I. Marquez, N. H. Slobodianik, P. A. Ronayne de Ferrer, A. R. Carlini, D. F. Vergani, and G. A. Daneri (1995). Immunoglobulin A levels in southern elephant seal (Mirounga leonina) milk during the suckling period. Comp. Biochem. Physiol. B112:569–572.Google Scholar
  102. 102.
    R. Jenness (1979). Comparative aspects of milk proteins. J. Dairy Res. 46:197–210.Google Scholar
  103. 103.
    K. Ohta, T. Watarai, T. Oishi, Y. Ueshiba, S. Hirose, T. Yoshizawa, Y. Akikusa, M. Sato, and H. Okano (1955). Composition of fin whale milk. Sci. Rep. Whales Res. Inst. 10:151–167.Google Scholar
  104. 104.
    M. Begg (1947). Ascorbic acid content of whale's milk. Nature 160:430.Google Scholar
  105. 105.
    J. P. Y. Arnould, I. L. Boyd, and D. G. Socha (1996). Milk consumption and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups. Can. J. Zool. 74:254–266.Google Scholar
  106. 106.
    J. L. Linzell (1972). Milk yield, energy loss in milk, and mammary gland weight in different species. Dairy Sci. Dairy Sci. Abstr. 34:351–360.Google Scholar
  107. 107.
    A. Hanwell and M. Peaker (1977). Physiological effects of lactation on the mother. Symp. Zool. Soc. Lond. 41:297–312.Google Scholar
  108. 108.
    C. W. Turner (1952). The Mammary Gland: The Anatomy of the Udder of Cattle and Domestic Animals. Lucas Brother Publishers, Columbia, Missouri.Google Scholar
  109. 109.
    R. M. Laws (1961). Reproduction, growth and age of southern fin whales. Discov. Rep. 31:327–486.Google Scholar
  110. 110.
    R. Gambell (1968). Seasonal cycles and reproduction in sei whales of the southern hemisphere. Discov. Rep. 35:31–134.Google Scholar
  111. 111.
    L. H. Matthews (1938). Notes on the southern right whale, Eubalaena australis. Discov. Rep. 17:169–182.Google Scholar
  112. 112.
    O. T. Oftedal (1981). Milk, protein and energy intakes of suckling mammalian young: a comparative study. Ph.D. thesis. Cornell University.Google Scholar
  113. 113.
    A. G. Tomilin (1946). Lactation and nutrition in cetaceans. Comptes Rendus(Doklady) Acad. Sci. URSS 52:277–279.Google Scholar
  114. 114.
    P. F. Brodie (1969). Duration of lactation in Cetacea: an indicator of required learning? Am. Midl. Natl. 82:312–314.Google Scholar
  115. 115.
    C. D. Tilden and O. T. Oftedal (1995). The bioenergetics of reproduction in prosimian primates: Is it related to female dominance? In L. Alterman (ed.), Creatures of the Dark: Tne Nocturnal Prosimians, Plenum Press, New York.Google Scholar
  116. 116.
    P. F. Frankland and F. J. Hambly (1890). The composition of the milk of the bottle-nose whale (Globicephalus melas). Chem. News J. Phys. Sci. 61:63.Google Scholar
  117. 117.
    L. Eichelberger, E. S. Fetcher, E. M. K. Geiling, and B. J. Vos (1940). The composition of dolphin milk. J. Biol. Chem. 134:171–176.Google Scholar
  118. 118.
    H. W. Symons and R. D. Weston (1958). Studies on the humpback whale (Megaptera nodosa) in the Bellingshausen Sea. Norsk Hvalfangst-Tid. 47:53–81.Google Scholar
  119. 119.
    J. F. Allen (1977). Dolphin reproduction in oceanaria in Australasia and Indonesia. In S. H. Ridgway and K. Benirschke (eds.), Breeding Dolphins: Present Status, Suggestions for the Future, US Marine Mammal Commission, Washington, D.C., pp. 85–108.Google Scholar
  120. 120.
    J. Clowes (1929). Southern blue and fin whales. Appendix I. A note on the composition of whale milk. Discov. Rep. 1:257–540.Google Scholar
  121. 121.
    P. Backhaus (1904). Zusammensetzung der Walmilch. Berlin Molkerei-Z. 14:481.Google Scholar
  122. 122.
    P. Backhaus (1904). Zusammensetzung der Walmilch. Österreich. Molkerei-Z. 11:279.Google Scholar
  123. 123.
    E. F. Heyerdahl (1930). Om sammensetningen av hvaldyrenes melk og om forholdene ved deres laktasjon. Publication No. 8, Kommandoer Christian Christenses Hvalfangstmuseum, Sandefjord, Norway.Google Scholar
  124. 124.
    S. Schmidt-Nielsen and F. Frog (1933). On the composition of the fat from a sample of whale milk. Kongl. Norske Vidensk. Selskab Forhandlinger 6:127–129.Google Scholar
  125. 125.
    P. B. Best (1960). Further information on Bryde's whale (Balaenoptera edeniAnderson) from Saldanha Bay, South Africa. Norsk Hvalfangst-Tid. 49:201–215.Google Scholar
  126. 126.
    T. Pedersen (1952). A note on humpback oil and on the milk and milk fat from this species (Megaptera nodosa). Norsk Hvalfangst-Tid. 41:375–378.Google Scholar
  127. 127.
    F. Wilke, T. Taniwaki, and N. Kuboda (1953). Phocoenoidesand Lagenorhynchusin Japan, with notes on hunting. J. Mammal. 34:488–497.Google Scholar

Copyright information

© Plenum Publishing Corporation 1997

Authors and Affiliations

  1. 1.Department of Zoological ResearchSmithsonian InstitutionWashington, D.C

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