The Influences of Environment, Mating Habitat, and Predation on Evolution of Pinniped Lactation Strategies


Seals have adapted their social systems and lactation strategies to marine environments that include open and ice-covered oceans, high and low productivity, extremes in seasonality, and ocean- and terrestrial-type predators. Different explanations for the variation in pinniped lactation systems have been proposed but tests of alternative hypotheses have not sufficiently accounted for phylogeny and body size. After controlling for this variation, I predicted that environment, mating habitat, and predation would yield a fuller explanation. Lactation traits, duration, pup growth rate, and fat content were significantly influenced by both body size and phylogeny, which together explained 20–69% of the variation. After controlling for this variation, initial results did not support the environment hypothesis, as no differences in lactation traits were found between species living in polar (≥60°N) versus equatorial (<60°N) environments. In contrast, seals that nurse in areas of Arctic sea ice contending with ice-hunting predators, such as polar bears, had relatively short lactation compared to species living in the Antarctic and more equatorial regions. Also, the availability of predator-free islands for terrestrial mating and parturition was related to a harem mating system, increased sexual size dimorphism (SSD), and slow juvenile growth rates, less fat in milk, and longer lactation. Using structural equation modeling, latitude and size of harems provided independent explanations for all three lactation traits. Thus, use of islands in ice-free waters, predation in Arctic ice-covered waters, and more milk fat in high-latitude seals together provided adequate explanations for the evolution of lactation diversity among pinnipeds.


Body size comparative method independent contrasts latitude path analysis seasonality sea ice seals sexual size dimorphism structural equation modeling temperature 


  1. Anderson, D. R., Burnham, K. P., and Thompson, W. L. (2000). Null hypothesis testing: Problems, prevalence, and an alternative. J. Wildl. Manage. 64: 912–923.CrossRefGoogle Scholar
  2. Atkinson, S. (1997). Reproductive biology of seals. Rev. Reproduction 2: 175–194.PubMedCrossRefGoogle Scholar
  3. Bartholomew, G. A. (1970). A model for the evolution of pinniped polygyny. Evolution 24: 546–559.CrossRefGoogle Scholar
  4. Bentler, P. M. (1983). Some contributions to efficient statistics in structural models: Specification and estimation of moment structures. Psychometrika 48: 493–517.CrossRefGoogle Scholar
  5. Bininda-Emonds, O. R. P. (2004a). The evolution of supertrees. Trends Ecol. Evol. 19: 315–322.PubMedCrossRefGoogle Scholar
  6. Bininda-Emonds, O. R. P. (2004b). Trees versus characters and the supertree/supermatrix “paradox.” Syst. Biol. 53: 356–359.PubMedCrossRefGoogle Scholar
  7. Bininda-Emonds, O. R. P., Gittleman, J. L., and Purvis, A. (1999). Building large trees by combining phylogenetic information: A complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74: 143–175.PubMedCrossRefGoogle Scholar
  8. Bininda-Emonds, O. R. P., Gittleman, J. L., and Steel, M. A. (2002). The (super)tree of life: Procedures, problems, and prospects. Annu. Rev. Ecol. Syst. 33: 265–289.CrossRefGoogle Scholar
  9. Blomberg, S. P., Garland, T., Jr., and Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57: 717–745.PubMedGoogle Scholar
  10. Boness, D. J. (1991). Determinants of mating systems in the Otariidae (Pinnipedia). In: The Behaviour of Pinnipeds, D. Renouf, ed., pp. 1–44, Chapman and Hall, London, UK.Google Scholar
  11. Boness, D. J., and Bowen, W. D. (1996). The evolution of maternal care in pinnipeds. BioScience 46: 645–654.CrossRefGoogle Scholar
  12. Bonner, W. N. (1984). Lactation strategies in pinnipeds: Problems for a marine mammalian group. Symp. Zool. Soc. Lond. 51: 253–272.Google Scholar
  13. Boyd, I. L. (1991). Environmental and physiological factors controlling the reproductive cycles of pinnipeds. Can. J. Zool. 69: 1135–1148.CrossRefGoogle Scholar
  14. Boyd, I. L. (1998). Time and energy constraints in pinniped lactation. Am. Nat. 152: 717–728.CrossRefPubMedGoogle Scholar
  15. Bowen, W. D., Oftedal, O. T., and Boness, D. J. (1985). Birth to weaning in 4 days: Remarkable growth in the hooded seal, Cystophora cristata. Can. J. Zool. 63: 2841–2846.CrossRefGoogle Scholar
  16. Bowen, W. D., Iverson, S. J., Boness, D. J., and Oftedal, O. T. (2001). Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Funct. Ecol. 15: 325–334.CrossRefGoogle Scholar
  17. Bozdogan, H. (1987). Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions. Psychometrika 52: 345–370.CrossRefGoogle Scholar
  18. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85: 1771–1789.CrossRefGoogle Scholar
  19. Burnham, K. P., and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer, New York.Google Scholar
  20. Calder, W. A., III (1984). Size, Function and Life History, Harvard University Press, Cambridge, UK.Google Scholar
  21. Caudron, A. K. (1997). Pinnipeds social systems: A review. Mammalia 61: 153–160.CrossRefGoogle Scholar
  22. Costa, D. P. (1991). Reproductive and foraging energetics of high latitude penguins, albatrosses and pinnipeds: Implications for life history patterns. Am. Zool. 31: 111–130.Google Scholar
  23. Davis, C. S., Delisle, I., Stirling, I., Siniff, D. B., and Strobeck, C. (2004). A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. Mol. Phylogenet. Evol. 33: 363–377.PubMedCrossRefGoogle Scholar
  24. Deecke, V. B., Slater, P. J. B., and Ford, J. K. B. (2002). Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420: 171–173.PubMedCrossRefGoogle Scholar
  25. Delisle, I., and Strobeck, C. (2005). A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol. Phylogenet. Evol. 37: 192–201.PubMedCrossRefGoogle Scholar
  26. Emlen, S. T., and Oring, L. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197: 215–233.PubMedCrossRefGoogle Scholar
  27. Estrada, J. A., Rice, A. N., Lutcavage, M. E., and Skomal, G. B. (2004). Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J. Mar. Biol. Ass. U.K. 83: 1347–1350.CrossRefGoogle Scholar
  28. Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125: 1–15.CrossRefGoogle Scholar
  29. Ferguson, S. H. (2002). Using survivorship curves to estimate age of first reproduction in moose Alces alces. Wildl. Biol. 8: 129–136.Google Scholar
  30. Ferguson, S. H., and Larivière, S. (2004). Are long penis bones an adaptation to high latitude snowy environments? Oikos 105: 255–267.CrossRefGoogle Scholar
  31. Ferguson, S. H., Virgl, J. A., and Larivière, S. (1996). Evolution of delayed implantation and associated grade shifts in life history traits of North American carnivores. Ecoscience 3: 7–17.Google Scholar
  32. Furgal, C. M., Innes, S., and Kovacs, K. M. (1996). Characteristics of ringed seal Phoca hispida, subnivean structures and breeding habitat and their effects on predation. Can. J. Zool. 74: 855–874.CrossRefGoogle Scholar
  33. Furgal, C. M., Innes, S., and Kovacs, K. M. (2002). Inuit spring hunting techniques and local knowledge of the ringed seal in Arctic Bay (Ilkpiarjuk), Nunavut. Pol. Res. 21: 1–16.CrossRefGoogle Scholar
  34. Garland, T., Jr., Dickerman, A. W., Janis, C. M., and Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42: 265–292.CrossRefGoogle Scholar
  35. Garland, T., Jr., Midford, P. E., and Ives, A. R. (1999). An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am. Zool. 39: 374–488.Google Scholar
  36. Garland, T., Jr., Midford, P. E., Jones, J. A., Dickerman, A. W., and Diaz-Uriarte, R. (2001). PDAP: Phenotypic Diversity Analysis Programs, Version 6.0, University of California, California.Google Scholar
  37. Gatesy, J., and Springer, M. (2005). A critique of matrix representation with parsimony supertrees. In: Phylogenetic Supertrees: Combining Information to Reveal the Tree of Life, O. R. P. Bininda-Emonds, ed., pp. 369–388, Computational Biology Series, Kluwer Academic, Dordrecht, The Netherlands.Google Scholar
  38. Gatesy, J., Matthee, C., DeSalle, R., and Hayashi, C. (2002). Resolution of a supertree/supermatrix paradox. Syst. Biol. 51: 652–664.PubMedCrossRefGoogle Scholar
  39. Gatesy, J., Baker, R. H., and Hayashi, C. (2004). Inconsistencies in arguments for the supertree approach: Supermatrices versus supertrees of Crocodylia. Syst. Biol. 53: 342–355.PubMedCrossRefGoogle Scholar
  40. Gittleman, J. L., and Oftedal, O. T. (1987). Comparative growth and lactation energetics in carnivores. Symp. Zool. Soc. Lond. 57: 41–77.Google Scholar
  41. Hairston, N. G., Jr., and Hairston, N. G., Sr. (1993). Cause–effect relationships in energy flow, trophic structure, and interspecific interactions. Am. Nat. 142: 379–411.CrossRefGoogle Scholar
  42. Harvey, P. H., and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology, Oxford University Press, Oxford, UK.Google Scholar
  43. Heise, K., Barrett-Lennard, L. G., Saulitis, E., Matkin, C., and Bain, D. (2003). Examining the evidence for killer whale predation on Steller sea lions in British Columbia and Alaska. Aquatic Mamm. 29: 325–334.CrossRefGoogle Scholar
  44. Jenness, R., and Sloan, R. E. (1970). The composition of milks of various species: A review. Dairy Sci. Abst. 32: 599–612.Google Scholar
  45. Kangas, A. T., Evans, A. R., Thesleff, I., and Jernvall, J. (2004). Nonindependence of mammalian dental characters. Nature 432: 211–214.PubMedCrossRefGoogle Scholar
  46. Kleiber, M. (1932). Body size and metabolism. Hilgardia 6: 315–332.Google Scholar
  47. Kovacs, K. M., and Lavigne, D. M. (1986). Maternal investment and neonatal growth in Phocid seals. J. Anim. Ecol. 55: 1035–1051.CrossRefGoogle Scholar
  48. Kovacs, K. M., and Lavigne, D. M. (1992). Maternal investment in otariid seals and walruses. Can. J. Zool. 70: 1953–1964.CrossRefGoogle Scholar
  49. Lindenfors, P., Tullberg, B. S., and Biuw, M. (2002). Phylogenetic analysis of sexual selection and sexual size dimorphism. Behav. Ecol. Sociobiol. 52: 188–193.CrossRefGoogle Scholar
  50. Lima, S. L. (2002). Putting predators back into behavioural predator–prey interactions. Trends Ecol. Evol. 17: 70–75.CrossRefGoogle Scholar
  51. Lydersen, C., and Hammill, M. O. (1993). Activity, milk intake and energy consumption in free-living ringed seal (Phoca hispida) pups. J. Comp. Phys. B Biochem. Syst. Environ. Phys. 163: 433–438.Google Scholar
  52. McIntire, E. J. B. (2004). Understanding natural disturbance boundary formation using spatial data and path analysis. Ecology 85: 1933–1943.CrossRefGoogle Scholar
  53. Millar, J. S. (1977). Adaptive features of mammalian reproduction. Evolution 31: 370–386.CrossRefGoogle Scholar
  54. Oftedal, O. T., Boness, D. J., and Tedman, R. A. (1987). The behaviour, physiology, and anatomy of lactation in the pinnipedia. Current Mamm. 1: 175–245.Google Scholar
  55. Partridge, L., and Harvey, P. H. (1988). The ecological context of life history evolution. Science 241: 1449–1455.PubMedCrossRefGoogle Scholar
  56. Petraitis, P. S., Dunham, A. E., and Niewiarowski, P. H. (1996). Inferring multiple causality: The limitations of path analysis. Funct. Ecol. 10: 421–431.CrossRefGoogle Scholar
  57. Purvis, A. (1995). A composite estimate of primate phylogeny. Philos. Trans. R. Soc. Lond. B 348: 405–421.CrossRefGoogle Scholar
  58. Pond, C. M. (1977). The significance of lactation in the evolution of mammals. Evolution 31: 177–199.CrossRefGoogle Scholar
  59. Quinn, J. F., and Dunham, A. E. (1983). On hypothesis testing in ecology and evolution. Am. Nat. 122: 602–617.CrossRefGoogle Scholar
  60. Ralls, K. (1977). Sexual dimorphism in mammals: Avian models and unanswered questions. Am. Nat. 981: 917–938.CrossRefGoogle Scholar
  61. SAS Institute (1999). SAS/STAT ® Users Guide, Version 6, SAS Institute, Cary, USA.Google Scholar
  62. Schulz, T. M., and Bowen, W. D. (2004). Pinniped lactation strategies: Evaluation of data on maternal and offspring life history traits. Mar. Mamm. Sci. 20: 86–114.CrossRefGoogle Scholar
  63. Schulz, T. M., and Bowen, W. D. (2005). The evolution of lactation strategies in pinnipeds: A phylogenetic analysis. Ecol. Monogr. 75: 159–177.CrossRefGoogle Scholar
  64. Schwarz, G. (1978). Estimating the dimension of a model. Ann. Stat. 6: 461–464.CrossRefGoogle Scholar
  65. Shipley, B. (2000). Cause and Correlation in Biology: A Users Guide to Path Analysis, Structural Equations and Causal Inference, Cambridge University Press, Cambridge, U.K.Google Scholar
  66. Sih, A. (1985). Evolution, predator avoidance and unsuccessful predation. Am. Nat. 125: 153–157.CrossRefGoogle Scholar
  67. Smith, T. G. (1976). Predation of ringed seal pups (Phoca hispida) by the Arctic fox (Alopex lagopus). Can. J. Zool. 54: 1610–1616.CrossRefGoogle Scholar
  68. Sokal, R. R., and Rohlf, F. J. (1995). Biometry, W. H. Freeman, San Francisco, USA.Google Scholar
  69. Springer, M. S., and de Jong, W. W. (2001). Which mammalian supertree to bark up? Science 291: 1710–1711.CrossRefGoogle Scholar
  70. Stewart, B. E., Innes, S., and Stewart, R. E. A. (1998). Mandibular dental ontogeny of ringed seals (Phoca hispida). Mar. Mamm. Sci. 14: 221–231.CrossRefGoogle Scholar
  71. Stirling, I. (1975). Factors affecting the evolution of social behaviour in the pinnipedian. Rapports et Proces-Verbaux des Reunions Cousel International Pour Lexplora de la Mer 169: 205–212.Google Scholar
  72. Stirling, I. (1977). Adaptations of Weddell and ringed seals to exploit the polar fast ice habitat in the absence and presence of surface predators. In: Adaptations Within Antarctic Ecosystems. Proceedings 3rd SCAR Symposium on Antarctic Biology, Washington, DC, August 26–30, 1974, G. A. Llano, ed., pp. 741–748, Gulf Publishing Company, Houston, USA.Google Scholar
  73. Stirling, I. (1983). The evolution of mating systems in pinnipeds. In: Advances in the Study of Mammalian Behaviour, J. F. Eisenberg, ed., pp. 489–527, Am. Soc. Mammal., Special Publication No. 7.Google Scholar
  74. Thornthwaite, C. W., and Mather, J. R. (1957). Instructions and tables for computing potential evapotranspiration and the water balance. Drexel Institute of Technology, Laboratory of Climatology. Publ. Climat. 10: 181–311.Google Scholar
  75. Trivers, R. L. (1972). Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, B. Campbell, ed., pp. 136–179, Aldine Press, Chicago, USA.Google Scholar
  76. Van Parijs, S. M. (2003). Aquatic mating in pinnipeds: A review. Aquatic Mamm. 29: 214–226.CrossRefGoogle Scholar
  77. Wilmott, C. J., Rowe, C. M., and Mintz, Y. (1985). Climatology of the terrestrial seasonal water cycle. J. Climatol. 5: 589–606.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Fisheries & OceansWinnipegCanada

Personalised recommendations