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

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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.

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LITERATURE CITED

  • 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.

    Article  Google Scholar 

  • Atkinson, S. (1997). Reproductive biology of seals. Rev. Reproduction 2: 175–194.

    Article  PubMed  CAS  Google Scholar 

  • Bartholomew, G. A. (1970). A model for the evolution of pinniped polygyny. Evolution 24: 546–559.

    Article  Google Scholar 

  • Bentler, P. M. (1983). Some contributions to efficient statistics in structural models: Specification and estimation of moment structures. Psychometrika 48: 493–517.

    Article  Google Scholar 

  • Bininda-Emonds, O. R. P. (2004a). The evolution of supertrees. Trends Ecol. Evol. 19: 315–322.

    Article  PubMed  Google Scholar 

  • Bininda-Emonds, O. R. P. (2004b). Trees versus characters and the supertree/supermatrix “paradox.” Syst. Biol. 53: 356–359.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

  • Boness, D. J., and Bowen, W. D. (1996). The evolution of maternal care in pinnipeds. BioScience 46: 645–654.

    Article  Google Scholar 

  • Bonner, W. N. (1984). Lactation strategies in pinnipeds: Problems for a marine mammalian group. Symp. Zool. Soc. Lond. 51: 253–272.

    Google Scholar 

  • Boyd, I. L. (1991). Environmental and physiological factors controlling the reproductive cycles of pinnipeds. Can. J. Zool. 69: 1135–1148.

    Article  Google Scholar 

  • Boyd, I. L. (1998). Time and energy constraints in pinniped lactation. Am. Nat. 152: 717–728.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bozdogan, H. (1987). Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions. Psychometrika 52: 345–370.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Burnham, K. P., and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer, New York.

  • Calder, W. A., III (1984). Size, Function and Life History, Harvard University Press, Cambridge, UK.

  • Caudron, A. K. (1997). Pinnipeds social systems: A review. Mammalia 61: 153–160.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Emlen, S. T., and Oring, L. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197: 215–233.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125: 1–15.

    Article  Google Scholar 

  • Ferguson, S. H. (2002). Using survivorship curves to estimate age of first reproduction in moose Alces alces. Wildl. Biol. 8: 129–136.

    Google Scholar 

  • Ferguson, S. H., and Larivière, S. (2004). Are long penis bones an adaptation to high latitude snowy environments? Oikos 105: 255–267.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

  • 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.

  • Gatesy, J., Matthee, C., DeSalle, R., and Hayashi, C. (2002). Resolution of a supertree/supermatrix paradox. Syst. Biol. 51: 652–664.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gittleman, J. L., and Oftedal, O. T. (1987). Comparative growth and lactation energetics in carnivores. Symp. Zool. Soc. Lond. 57: 41–77.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Harvey, P. H., and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology, Oxford University Press, Oxford, UK.

  • 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.

    Article  Google Scholar 

  • Jenness, R., and Sloan, R. E. (1970). The composition of milks of various species: A review. Dairy Sci. Abst. 32: 599–612.

    Google Scholar 

  • Kangas, A. T., Evans, A. R., Thesleff, I., and Jernvall, J. (2004). Nonindependence of mammalian dental characters. Nature 432: 211–214.

    Article  PubMed  CAS  Google Scholar 

  • Kleiber, M. (1932). Body size and metabolism. Hilgardia 6: 315–332.

    CAS  Google Scholar 

  • Kovacs, K. M., and Lavigne, D. M. (1986). Maternal investment and neonatal growth in Phocid seals. J. Anim. Ecol. 55: 1035–1051.

    Article  Google Scholar 

  • Kovacs, K. M., and Lavigne, D. M. (1992). Maternal investment in otariid seals and walruses. Can. J. Zool. 70: 1953–1964.

    Article  Google Scholar 

  • Lindenfors, P., Tullberg, B. S., and Biuw, M. (2002). Phylogenetic analysis of sexual selection and sexual size dimorphism. Behav. Ecol. Sociobiol. 52: 188–193.

    Article  Google Scholar 

  • Lima, S. L. (2002). Putting predators back into behavioural predator–prey interactions. Trends Ecol. Evol. 17: 70–75.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • McIntire, E. J. B. (2004). Understanding natural disturbance boundary formation using spatial data and path analysis. Ecology 85: 1933–1943.

    Article  Google Scholar 

  • Millar, J. S. (1977). Adaptive features of mammalian reproduction. Evolution 31: 370–386.

    Article  Google Scholar 

  • 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 

  • Partridge, L., and Harvey, P. H. (1988). The ecological context of life history evolution. Science 241: 1449–1455.

    Article  PubMed  Google Scholar 

  • Petraitis, P. S., Dunham, A. E., and Niewiarowski, P. H. (1996). Inferring multiple causality: The limitations of path analysis. Funct. Ecol. 10: 421–431.

    Article  Google Scholar 

  • Purvis, A. (1995). A composite estimate of primate phylogeny. Philos. Trans. R. Soc. Lond. B 348: 405–421.

    Article  CAS  Google Scholar 

  • Pond, C. M. (1977). The significance of lactation in the evolution of mammals. Evolution 31: 177–199.

    Article  Google Scholar 

  • Quinn, J. F., and Dunham, A. E. (1983). On hypothesis testing in ecology and evolution. Am. Nat. 122: 602–617.

    Article  Google Scholar 

  • Ralls, K. (1977). Sexual dimorphism in mammals: Avian models and unanswered questions. Am. Nat. 981: 917–938.

    Article  Google Scholar 

  • SAS Institute (1999). SAS/STAT ® Users Guide, Version 6, SAS Institute, Cary, USA.

  • 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.

    Article  Google Scholar 

  • Schulz, T. M., and Bowen, W. D. (2005). The evolution of lactation strategies in pinnipeds: A phylogenetic analysis. Ecol. Monogr. 75: 159–177.

    Article  Google Scholar 

  • Schwarz, G. (1978). Estimating the dimension of a model. Ann. Stat. 6: 461–464.

    Article  Google Scholar 

  • 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.

  • Sih, A. (1985). Evolution, predator avoidance and unsuccessful predation. Am. Nat. 125: 153–157.

    Article  Google Scholar 

  • Smith, T. G. (1976). Predation of ringed seal pups (Phoca hispida) by the Arctic fox (Alopex lagopus). Can. J. Zool. 54: 1610–1616.

    Article  Google Scholar 

  • Sokal, R. R., and Rohlf, F. J. (1995). Biometry, W. H. Freeman, San Francisco, USA.

  • Springer, M. S., and de Jong, W. W. (2001). Which mammalian supertree to bark up? Science 291: 1710–1711.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

  • 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.

  • 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 

  • 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.

  • Van Parijs, S. M. (2003). Aquatic mating in pinnipeds: A review. Aquatic Mamm. 29: 214–226.

    Article  Google Scholar 

  • Wilmott, C. J., Rowe, C. M., and Mintz, Y. (1985). Climatology of the terrestrial seasonal water cycle. J. Climatol. 5: 589–606.

    Article  Google Scholar 

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ACKNOWLEDGMENTS

NSERC Discovery Grant (250465-03) and ArcticNet supported this research. Earlier drafts of this paper were greatly improved by discussions and critical reviews by the editor, M. S. Springer, an anonymous reviewer, W. D. Bowen, and R. E. A. Stewart.

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Correspondence to Steven H. Ferguson.

 

 

Appendix 1. Traits and Environmental Measures for 34 Pinniped Species

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Ferguson, S.H. The Influences of Environment, Mating Habitat, and Predation on Evolution of Pinniped Lactation Strategies. J Mammal Evol 13, 63–82 (2006). https://doi.org/10.1007/s10914-005-9003-1

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