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How seals divide up the world: environment, life history, and conservation

  • GLOBAL CHANGE AND CONSERVATION ECOLOGY
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Abstract

Pinnipeds display a remarkable variation in life history adaptations while successfully inhabiting almost every marine environment. We explore how they have done this by grouping the world’s pinniped species according to their environmental conditions, mating systems, lactation strategies, and timing of life histories. Next, we tested whether any of these clusters provide information about risk of extinction (using the International Union for Nature and the Conservation of Natural Resources status ranks). Seals at risk were not characterized by differences in lactation pattern (22% short vs. 46% long), mating system (24% multi-male vs. 35% harems), or timing of life history events (23% fast vs. 42% slow) but did differ based on four environmental groupings. Grouping traits (rather than seals) described two clusters: one that included the environmental trait, primary productivity, and a second one that included all other environmental variables (seasonality, latitude, and temperature). Based on this result and theoretical considerations, we plotted seals according to energy (primary productivity) and variation (seasonality) and found a pattern analogous to that of the same four groups determined by cluster analysis of all environmental variables. Of the two pinniped groups representing low variation (equatorial and high productivity), ten of 21 seal species have been designated at risk, in contrast to none of the 13 seal species adapted to high variation. We conclude that seals appear to be best adapted to seasonal environments and thus, conservation efforts may benefit by concentrating on species inhabiting less variable environments.

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References

  • Allen AP, Brown JH, Gillooly JF (2002) Global biodiversity, biochemical kinetics, and the energy-equivalence rule. Science 297:1545–1548

    Article  PubMed  CAS  Google Scholar 

  • Alroy J (2001) A multispecies overkill simulation of the end-Pleistocene megafaunal mass extinction. Science 292:1893–1896

    Article  PubMed  CAS  Google Scholar 

  • Ando A, Camm J, Polasky S, Solow A (1998) Species distribution, land values, and efficient conservation. Science 279:2126–2128

    Article  PubMed  CAS  Google Scholar 

  • Arnould JP, Boyd IL, Warneke RM (2003) Historical dynamics of the Australian fur seal population: evidence of regulation by man? Can J Zool 81:1428–1436

    Article  Google Scholar 

  • Barnes LG, Domning DP, Ray CE (1985) Status of studies on fossil marine mammals. Mar Mamm Sci 1:15–53

    Article  Google Scholar 

  • Behrenfeld MJ, Bale AJ, Kolber ZS, Aiken J, Falkowski PG (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383:508–511

    Article  CAS  Google Scholar 

  • Berta A, Sumich JL (1999) Marine mammals: evolutionary biology. Academic Press, San Diego, Calif.

    Google Scholar 

  • Bininda-Emonds ORP, Gittleman JL, 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 

  • Boness DJ, Clapham PJ, Mesnick SL (2002) Life history and reproductive strategies. In: Hoelzel R (ed) Marine mammal biology: an evolution approach. Blackwell, Oxford, pp 278–324

    Google Scholar 

  • Bowen WD (1991) Behavioural ecology of pinniped neonates. In: Renouf D (ed) The behaviour of pinnipeds. Chapman and Hall, London, pp 66–127

    Google Scholar 

  • Boyce MS (1979) Seasonality and patterns of natural selection for life histories. Am Nat 114:569–583

    Article  Google Scholar 

  • Branke J (2002) Evolutionary optimization in dynamic environments. Kluwer, Mass.

    Google Scholar 

  • Cardillo M, Purvis A, Sechrest W, Gittleman JL, Bielby J, Mace GM (2004) Human population density and extinction risk in the world’s carnivores. PLoS Biol 2:909–914

    Article  CAS  Google Scholar 

  • Ceballos G, Ehrlich PR (2002) Mammal population losses and the extinction crisis. Science 296:904–907

    Article  PubMed  CAS  Google Scholar 

  • Cheung WWL, Pitcher TJ, Pauly D (2005) A fuzzy logic expert system to estimate intrinsic extinction vulnerabilities of marine fishes to fishing. Biol Conserv 124:97–111

    Article  Google Scholar 

  • Costa DP (1993) The relationship between reproductive and foraging energetics and the evolution of the Pinnipedia. Sym Zool Soc Lond 66:293–314

    Google Scholar 

  • Costa DP, Kuhn CE, Weise MJ, Shaffer SA, Arnould JPY (2004) When does physiology limit the foraging behaviour of freely diving mammals? Int Congr Ser 1275:359–366

    Article  Google Scholar 

  • Deméré TA, Berta A, Adam PJ (2003) Pinnipedimorph evolutionary biogeography. Bull Am Mus Nat Hist 279:32–76

    Article  Google Scholar 

  • Donlan CJ, Knowlton J, Doak DF (2005) Nested communities, invasive species and Holocene extinctions: evaluating the power of a potential conservation tool. Oecologia 145:475–485

    Article  PubMed  Google Scholar 

  • Dulvy NK, Ellis JR, Goodwin NB, Grant A, Reynolds JD, Jennings S (2004) Methods of assessing extinction risk in marine fishes. Fish Fish 5:255–276

    Google Scholar 

  • Eberhardt LL, Siniff DB (1977) Population dynamics and marine mammal management policies. J Fish Res Bd Can 34:183–190

    Google Scholar 

  • Engelhard GH, Baarspul ANJ, Broekman M, Creuwels ANJ, Reijnders PJH (2002) Human disturbances, nursing behaviour, and lactation of pup growth in a declining southern elephant seal (Mirounga leonina) population. Can J Zool 80:1876–1886

    Article  Google Scholar 

  • Fay FH, Kelly BP, Sease JL (1989) Managing the exploitation of Pacific walruses: a tragedy of delayed response and poor communication. Mar Mamm Sci 5:1–16

    Article  Google Scholar 

  • Ferguson SH (2002) The effects of productivity and seasonality on life history: comparing age at maturity among moose (Alces alces) populations. Global Ecol Biogeogr 11:303–312

    Article  Google Scholar 

  • Ferguson SH (2006) The influences of environment, mating habitat, and predation on evolution of pinniped lactation strategies. J Mamm Evol 13:63–82

    Article  Google Scholar 

  • Ferguson SH, Larivière S (2002) Can comparing life histories help conserve carnivores? Anim Conserv 5:1–12

    Google Scholar 

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

    Article  Google Scholar 

  • Ferguson SH, McLoughlin PD (2000) Effect of energy availability, seasonality, and geographic range on brown bear life-history. Ecography 23:193–200

    Article  Google Scholar 

  • Ferguson SH, Virgl JA, Larivière S (1996) Evolution of delayed implantation and associated grade shifts in life history traits of North American carnivores. Ècoscience 3:7–17

    Google Scholar 

  • Fisher DO, Owens IPF (2004) The comparative method in conservation biology. Trends Ecol Evol 19:391–398

    Article  PubMed  Google Scholar 

  • Fodor JA (1983) Précis of the modularity of mind. Behav Brain Sci 8:1–42

    Article  Google Scholar 

  • Fowler CW (1981) Density dependence as related to life history strategy. Ecology 62:602–610

    Article  Google Scholar 

  • Fowler CW (1990) Density dependence in northern fur seals (Callorhinus ursinus). Mar Mamm Sci 6:171–195

    Article  Google Scholar 

  • Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Article  Google Scholar 

  • Garland T Jr, Midford PE, Ives AR (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 

  • Gerber LR, Hilborn R (2001) Catastrophic events and recovery from low densities in populations of otariids: implications for risk of extinction. Mamm Rev 31:131–150

    Article  Google Scholar 

  • Harwood J, Rohani P (1996) The population biology of marine mammals. In: Floyd RB, Sheppard AW, DeBarro PJ (eds) Frontiers of population ecology. CSIRO, Melbourne, pp 173–190

    Google Scholar 

  • Harvey PH, Godfray HCJ (1987) How species divide resources. Am Nat 129:318–320

    Article  Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Hindell MA (1991) Some life-history parameters of a declining population of Southern elephant seals, Mirounga leonina. J Anim Ecol 60:119–134

    Article  Google Scholar 

  • Hindell MA, Bradshaw CJA, Sumner MD, Michael KJ, Burton HR (2003) Dispersal of female southern elephant seals and their prey consumption during the austral summer: relevance to management and oceanographic zones. J Appl Ecol 40:703–715

    Article  Google Scholar 

  • Hucke-Gaete R, Osman LP, Moreno CA, Torres D (2004) Examining natural population growth from near extinction: the South Shetlands, Antarctica. Polar Biol 27:304–311

    Article  Google Scholar 

  • IUCN (International Union for Conservation of Nature and Natural Resources) (1996) Red list of threatened animals. IUCN, Gland, Switzerland

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Senihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  PubMed  CAS  Google Scholar 

  • Jennings S, Reynolds JD, Mills SC (1998) Life history correlates of responses to fisheries exploitation. Proc R Soc Lond Biol Sci 265:333–339

    Article  Google Scholar 

  • Jennings S, Reynolds JD, Polunin NVC (1999) Predicting the vulnerability of tropical reef fishes to exploitation with phylogenies and life histories. Conserv Biol 13:1466–1475

    Article  Google Scholar 

  • Klein RG (2000) Human evolution and large mammal extinctions. In: Vrba ES, Schaller GB (eds) Antelopes, deer, and relatives, present and future: fossil record, behavioral ecology, systematics, and conservation. Yale University Press, New Haven, pp 128–139

    Google Scholar 

  • Klingenberg CP (2002) Morphometrics and the role of the phenotype in studies of the evolution of developmental mechanisms. Gene 287:3–10

    Article  PubMed  CAS  Google Scholar 

  • Kotiaho JS, Kaitala V, Komonen A, Päivinen J (2005) Predicting the risk of extinction from shared ecological characteristics. Proc Natl Acad Sci USA 102:1963–1967

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Liou LW, Price T, Boyce MS, Perrins CM (1993) Fluctuating environments and clutch size evolution in great tits. Am Nat 141:507–516

    Article  Google Scholar 

  • Mangel M, Talbot LM, Meffe GK, Agardy MT, Alverson DL, Barlow J, Botkin DB, Budowski G, Clark T, Cooke J, Crozier DB, Dayton PK, Elder DL, Fowler CW, Funtowicz S, Giske J, Hofman RJ, Holt SJ, Kellert SR, Kimball LA, Ludwig D, Magnusson K, Malayang BS III, Mann C, Norse EA, Northridge SP, Perrin WF, Perrings C, Peterman RM, Rabb GB, Reiger HA, Reynolds JE III, Sherman K, Sissenwine MP, Smith TD, Starfield A, Taylor RJ, Tillman MF, Toft C, Twiss JR Jr, Wilen J, Young TP (1996) Principles for the conservation of wild living resources. Ecol Appl 6:338–362

    Google Scholar 

  • McDonnell MJ, Pickett STA (Eds) (1993) Humans as components of ecosystems: the ecology of subtle human effects and populated areas. Springer, Berlin Heidelberg New York

  • McKee JK (2003) Sparing nature—the conflict between human population growth and earth’s biodiversity. Rutgers University Press, Piscataway

    Google Scholar 

  • McKee JK (2001) Faunal turnover rates and mammalian biodiversity of the Late Pliocene and Pleistocene of eastern Africa. Paleobiology 27:500–511

    Article  Google Scholar 

  • McKinney ML (1997) Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu Rev Ecol Syst 28:495–516

    Article  Google Scholar 

  • McMahon CR, Hindell MA, Burton HR, Beste MN (2005) Comparison of southern elephant seal populations, and observations of a population on a demographic knife-edge. Mar Ecol Prog Ser 288:273–283

    Google Scholar 

  • Menge BA, Southerland JP (1976) Species diversity gradients: synthesis of the role of predation, competition and temporal heterogeneity. Am Nat 110:351–369

    Article  Google Scholar 

  • Naves J, Wiegand T, Revilla E, Delibes D (2003) Endangered species constrained by natural and human factors: the case of brown bears in northern Spain. Conserv Biol 17:1276–1289

    Article  Google Scholar 

  • Norris K (2004) Managing threatened species: the ecological toolbox, evolutionary theory and declining-population paradigm. J Appl Ecol 41:413–426

    Article  Google Scholar 

  • Pastor T, Garza JC, Allen P, Amos W, Aguilar A (2004) Low genetic variability in the highly endangered Mediterranean Monk Seal. J Hered 95:291–300

    Article  PubMed  CAS  Google Scholar 

  • Pauly D, Christensen V, Guenette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418:689–695

    Article  PubMed  CAS  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Google Scholar 

  • Pistorius PA, Lewis MN, Bester MN, Campagna C, Kirkman SP, Taylor FE (2004) Adult female survival, population trend, and the implications of early primiparity in a capital breeder, the southern elephant seal (Mirounga leonina). J Zool Lond 263:107–119

    Google Scholar 

  • Pistorius PA, Bester MN, Kirkman SP, Taylor FE (2001) Temporal changes in fecundity and age of maturity in the southern elephant seal population at Marion Island. Polar Biol 24: 343–348

    Article  Google Scholar 

  • Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proc R Soc Lond Ser B 267:1947–1952

    Article  CAS  Google Scholar 

  • Raff RA, Sly BJ (2000) Modularity and dissociation in the evolution of gene expression territories in development. Evol Dev 2:102–113

    Article  PubMed  CAS  Google Scholar 

  • Reynolds JD, Jennings S, Dulvy NK (2001) Life histories of fishes and population responses to exploitation. In: Reynolds JD, Mace GM, Redford KH, Robinson JG (eds) Conservation of exploited species. Cambridge University Press, Cambridge, pp 147–169

    Google Scholar 

  • Riedman M (1990) The Pinnipeds: seals, sea lions, and walruses. University of California Press, Berkely, Calif.

    Google Scholar 

  • Romesburg HC (1984) Cluster analysis for researchers. Lifetime Learning, Belmont

    Google Scholar 

  • Sæther B-E (1988) Pattern of covariation between life-history traits of European birds. Nature 331:616–617

    Article  PubMed  Google Scholar 

  • Sæther B-E, Ringsby TH, Roskaft E (1996) Life-history variation, population processes and priorities in species conservation: towards a reunion of research paradigms. Okois 77:217–226

    Google Scholar 

  • SAS Institute (1999) SAS/STATusers guide, version 6. SAS Institute, Cary, N.C.

  • Schulz TM, Bowen WD (2004) Pinniped lactation strategies: evaluation of data on maternal and offspring life history traits. Mar Mamm Sci 20:86–114

    Article  Google Scholar 

  • Schulz TM, Bowen WD (2005) The evolution of lactation strategies in pinnipeds: a phylogenetic analysis. Ecol Mono 75:159–177

    Google Scholar 

  • Sibly R, Calow P (1985) Classification of habitats by selection pressures: a synthesis of life-cycle and r/K theory. In: Sibly RM, Smith RH (eds) Behavioural ecology. Blackwell, Oxford, pp 75–90

    Google Scholar 

  • Slobodkin LB, Sanders HL (1969) On the contribution of environmental predictability to species diversity. Brookhaven Symp Biol 22:82–95

    PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, San Francisco, Calif.

    Google Scholar 

  • Stevens GC (1989) The latitudinal gradient in geographic range: how so many species coexist in the tropics. Am Nat 133:240–256

    Article  Google Scholar 

  • Stewart BS, DeLong RL (1993) Seasonal dispersion and habitat use of foraging northern elephant seals. Symp Zool Soc Lond 66:179–194

    Google Scholar 

  • Sugihara G (1989) How do species divide resources? Am Nat 133:458–463

    Article  Google Scholar 

  • Tsydenova D, Minh TB, Kajlwara N, Botoev V, Tauabe S (2004) Recent contamination by persistent organochlorines in Baikal seal (Phoca sibirica) from Lake Baikal, Russia. Mar Poll Bull 48:749–758

    Article  CAS  Google Scholar 

  • Tuljapurkar SD (1990) Population dynamics in variable environments. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendii). J Hered 95:144–153

    Article  PubMed  CAS  Google Scholar 

  • Wickens P, York AE (1997) Comparative dynamics of fur seals. Mar Mamm Sci 13:241–292

    Article  Google Scholar 

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

    Google Scholar 

  • Wyss AR (1988) Evidence from flipper structure for a single origin of pinnipeds. Nature 334:427–428

    Article  Google Scholar 

  • Wyss AR (1994) The evolution of body size in phocids: some ontogenetic and phylogenetic observations. In: Berta A, Dmere TA (eds) Contributions in marine mammal paleontology honoring Franck C. Whitmore, jr., vol 29. Proceedings of the San Diego Society of Natural History, San Diego, Calif, pp 69–75

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Acknowledgements

An NSERC Discovery Grant (250465-03) and ArcticNet supported this research. M. Mangel and an anonymous reviewer improved earlier drafts of this paper.

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Correspondence to Steven H. Ferguson.

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Communicated by Craig Osenberg

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Ferguson, S.H., Higdon, J.W. How seals divide up the world: environment, life history, and conservation. Oecologia 150, 318–329 (2006). https://doi.org/10.1007/s00442-006-0489-x

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