Individual heterogeneity in reproductive rates and cost of reproduction in a long-lived vertebrate

Ecology and Evolution

Volumn 3, Issue 7, 2013, Pages 2047-2060

  Chambert, Thierry ^a   Rotella, Jay J ^a   Higgs, Megan D ^a   Garrott, Robert A ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

Bayesian statistics; Individual variation; Life history theory; Marine mammals; Population dynamics; Posterior predictive checks

Indexed keywords

EID: 84886241421     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.615     Document Type: Article

References (90)

1. Andersson, S. 1989. Sexual selection and cues for female choice in leks of Jackson's widowbird Euplectes jacksoni. Behav. Ecol. Sociobiol. 25:403-410.
2. Atkinson, S. 1997. Reproductive biology of seals. Rev. Reprod. 2:175-194.
3. Aubry, L. M., D. N. Koons, J.-Y. Monnat, and E. Cam 2009. Consequences of recruitment decisions and heterogeneity on age-specific breeding success in a long-lived seabird. Ecology 90:2491-2502.
4. Aubry, L. M., E. Cam, D. N. Koons, J.-Y. Monnat, and S. Pavard 2011. Drivers of age-specific survival in a long-lived seabird: contributions of observed and hidden sources of heterogeneity. J. Anim. Ecol. 80:375-383.
5. Barbraud, C., and H. Weimerskirch 2005. Environmental conditions and breeding experience affect costs of reproduction in blue petrels. Ecology 86:682-692.
6. Barnett, A. G., N. Koper, A. J. Dobson, F. Schmiegelow, and M. Manseau 2010. Using information criteria to select the correct variance-covariance structure for longitudinal data in ecology. Methods Ecol. Evol. 1:15-24.
7. Bergeron, P., R. Baeta, F. Pelletier, D. Réale, and D. Garant 2011. Individual quality: tautology or biological reality? J. Anim. Ecol. 80:361-364.
8. Bérubé, C. H., M. Festa-Bianchet, and J. T. Jorgenson 1999. Individual differences, longevity, and reproductive senescence in bighorn ewes. Ecology 80:2555-2565.
9. Boness, D. J., and W. D. Bowen 1996. The evolution of maternal care in pinnipeds. Bioscience 46:645-654.
10. Brooks, S. P., and A. Gelman 1998. General methods for monitoring convergence of iterative simulations. J. Comput. Graph. Stat. 7:434-455.
11. Burnham, K. P., and D. R. Anderson 2002. Model selection and multimodel inference, a practical information-theoretic approach. 2nd ed. Springer, New York.
12. Burns, J. M., S. J. Trumble, M. A. Castellini, and J. W. Testa 1998. The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol. 19:272-282.
13. Burton, T., S. S. Killen, J. D. Armstrong, and N. B. Metcalfe 2011. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc. Biol. Sci. 278:3465-3473.
14. Cam, E., and J.-Y. Monnat 2000. Apparent inferiority of first-time breeders in the kittiwake: the role of heterogeneity among age classes. J. Anim. Ecol. 69:380-394.
15. Cam, E., W. A. Link, E. G. Cooch, J. Monnat, and E. Danchin 2002. Individual covariation in life-history traits: seeing the trees despite the forest. Am. Nat. 159:96-105.
16. Cam, E., O. Gimenez, R. Alpizar-Jara, L. M. Aubry, M. Authier, E. G. Cooch, et al. 2012. Looking for a needle in a haystack: inference about individual fitness components in a heterogeneous population. Oikos. doi:10.1111/j.1600-0706.2012.20532.x
17. Cameron, M. F., and D. B. Siniff 2004. Age-specific survival, abundance, and immigration rates of a Weddell seal (Leptonychotes weddellii) population in McMurdo Sound, Antarctica. Can. J. Zool. 82:601-615.
18. Cameron, M. F., D. B. Siniff, K. M. Proffitt, and R. A. Garrott 2007. Site fidelity of Weddell seals: the effects of sex and age. Antarct. Sci. 19:149-155.
19. Carpenter, S. R. 1990. Large-scale perturbations: opportunities for innovation. Ecology 71:2038-2043.
20. Castellini, M. A., G. L. Kooyman, and P. J. Ponganis 1992. Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J. Exp. Biol. 165:181-194.
21. Chambert, T., J. J. Rotella, and R. A. Garrott 2012. Environmental extremes versus ecological extremes: impact of a massive iceberg on the population dynamics of a high-level Antarctic marine predator. Proc. Biol. Sci. 279: 4532-4541.
22. Conner, M. M., and G. C. White 1999. Effects of individual heterogeneity in estimating the persistence of small populations. Nat. Res. Model. 12:109-127.
23. Costa, D. P., C. Kuhn, M. Weise, S. Shaffer, and J. P. Y. Arnould 2004. When does physiology limit the foraging behaviour of freely diving mammals? Int. Congr. Ser. 1275:359-366.
24. Cubaynes, S., C. Lavergne, E. Marboutin, and O. Gimenez 2012. Assessing individual heterogeneity using model selection criteria: how many mixture components in capture-recapture models? Methods Ecol. Evol. 3:564-573.
25. Dall, S. R. X., A. I. Houston, and J. M. McNamara 2004. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7:734-739.
26. Darwin, C. 1859. On the origin of species by means of natural selection or the preservation of favored races in the struggle for life. J. Murray, London.
27. Endler, J. A. 1986. Natural selection in the wild. Princeton Univ. Press, New Jersey.
28. Festa-Bianchet, M., J. T. Jorgenson, C. H. Bérubé, C. Portier, and W. D. Wishart 1997. Body mass and survival of bighorn sheep. Can. J. Zool. 75:1372-1379.
29. Festa-Bianchet, M., J. T. Jorgenson, and D. Réale 2000. Early development, adult mass, and reproductive success in bighorn sheep. Behav. Ecol. 11:633-639.
30. Foerster, K., K. Delhey, A. Johnsen, J. T. Lifjeld, and B. Kempenaers 2003. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714-717.
31. Fox, G. A., B. E. Kendall, J. W. Fitzpatrick, and G. E. Woolfenden 2006. Consequences of heterogeneity in survival probability in a population of Florida scrub-jays. J. Anim. Ecol. 75:921-927.
32. Gelman, A., J. B. Carlin, H. S. Stern, and D. B. Rubin 2004. P.159 in Bayesian data analysis, 2nd ed. Boca Raton, Chapman & Hall/CRC.
33. Gimenez, O., and R. Choquet 2010. Individual heterogeneity in studies on marked animals using numerical integration: capture-recapture mixed models. Ecology 91:951-957.
34. Gould, S. J., and N. Eldredge 1993. Punctuated equilibrium comes of age. Nature 366:223-227.
35. Guglielmo, L., A. Granata, and S. Greco 1998. Spatial and temporal variability of size-fractionated biomass and primary production in the Ross Sea (Antarctica) during austral spring and summer. Polar Biol. 19:37-51.
36. Guglielmo, L., P. Donato, G. Zagami, and A. Granata 2009. Spatio-temporal distribution and abundance of Euphausia crystallorophias in Terra Nova Bay (Ross Sea, Antarctica) during austral summer. Polar Biol. 32:347-367.
37. Hadley, G. L., J. J. Rotella, R. A. Garrott, and J. D. Nichols 2006. Variation in probability of first reproduction of Weddell seals. J. Anim. Ecol. 75:1058-1070.
38. Hadley, G. L., J. J. Rotella, and R. A. Garrott 2007a. Evaluation of reproductive costs for Weddell seals in Erebus Bay, Antarctica. J. Anim. Ecol. 76:448-458.
39. Hadley, G. L., J. J. Rotella, and R. A. Garrott 2007b. Influence of maternal characteristics and oceanographic conditions on survival and recruitment probabilities of Weddell seals. Oikos 116:601-613.
40. Hamel, S., S. D. Côté, J.-M. Gaillard, and M. Festa-Bianchet 2009a. Individual variation in reproductive costs of reproduction: high-quality females always do better. J. Anim. Ecol. 78:143-151.
41. Hamel, S., J.-M. Gaillard, M. Festa-Bianchet, and S. D. Côté 2009b. Individual quality, early-life conditions, and reproductive success in contrasted populations of large herbivores. Ecology 90:1981-1995.
42. Hamel, S., J. M. Craine, and E. G. Towne 2012a. Maternal allocation in bison: co-occurrence of senescence, cost of reproduction, and individual quality. Ecol. Appl. 22:1628-1639.
43. Hamel, S., N. G. Yoccoz, and J.-M. Gaillard 2012b. Statistical evaluation of parameters estimating autocorrelation and individual heterogeneity in longitudinal studies. Methods Ecol. Evol. 3:731-742.
44. Hunt, J., and L. W. Simmons 2000. Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus. Evolution 54:936-941.
45. Hunt, J., L. F. Bussière, M. D. Jennions, and R. Brooks 2004. What is genetic quality? Trends Ecol. Evol. 19:329-333.
46. Kendall, B. E., G. A. Fox, M. Fujiwara, and T. M. Nogeire 2011. Demographic heterogeneity, cohort selection, and population growth. Ecology 92:1985-1993.
47. Kooyman, G. L., D. H. Kerem, W. B. Campbell, and J. J. Wright 1973. Pulmonary gas exchange in freely diving weddell seals Leptonychotes weddelli. Respir. Physiol. 17:283-290.
48. Lailvaux, S. P., and M. M. Kasumovic 2011. Defining individual quality over lifetimes and selective contexts. Proc. Biol. Sci. 278:321-328.
49. Landis, R. M., J. Gurevitch, G. A. Fox, W. E. I. Fang, and D. R. Taub 2005. Variation in recruitment and early demography in Pinus rigida following crown fire in the pine barrens of Long Island, New York. J. Ecol. 93:607-617.
50. Lescroël, A., K. M. Dugger, G. Ballard, and D. G. Ainley 2009. Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J. Anim. Ecol. 78:798-806.
51. Lindström, J. 1999. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14:343-348.
52. Link, W. A., and R. J. Barker 2010. Pp. 127-159 in Bayesian inference with ecological applications. Academic Press, London.
53. Link, W. A., E. G. Cooch, and E. Cam 2002. Model-based estimation of individual fitness. J. Appl. Stat. 29:207-224.
54. Lomnicki, A. 1978. Individual differences between animals and the natural regulation of their numbers. J. Anim. Ecol. 47:461-475.
55. Lummaa, V., and T. Clutton-Brock 2002. Early development, survival and reproduction in humans. Trends Ecol. Evol. 17:141-147.
56. Lunn, D., D. Spiegelhalter, A. Thomas, and N. Best 2009. The BUGS project: evolution, critique and future directions. Stat. Med. 28:3049-3067.
57. MacAyeal, D. R., M. H. Okal, J. E. Thom, K. M. Brunt, Y. -J. Kim, and A. K. Bliss 2008. Tabular iceberg collisions within the coastal regime J. Glaciol. 54:371-386.
58. Metcalfe, N. B., and P. Monaghan 2001. Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16:254-260.
59. Mousseau, T. A., and C. W. Fox 1998. The adaptive significance of maternal effects. Trends Ecol. Evol. 13:403-407.
60. Nussey, D. H., T. Coulson, M. Festa-Bianchet, and J.-M. Gaillard 2008. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22:393-406.
61. Oli, M., and K. Armitage 2003. Sociality and individual fitness in yellow-bellied marmots: insights from a long-term study (1962-2001). Oecologia 136:543-550.
62. Orzack, S. H., U. K. Steiner, S. Tuljapurkar, and P. Thompson 2011. Static and dynamic expression of life history traits in the northern fulmar Fulmarus glacialis. Oikos 120:369-380.
63. Plard, F., C. Bonenfant, D. Delorme, and J. M. Gaillard 2012. Modeling reproductive trajectories of roe deer females: fixed or dynamic heterogeneity? Theor. Popul. Biol. 82:317-328.
64. Pryke, S. R., L. B. Astheimer, S. C. Griffith, and W. A. Buttemer 2012. Covariation in life-history traits: differential effects of diet on condition, hormones, behavior, and reproduction in genetic finch morphs. Am. Nat. 179:375-390.
65. Rotella, J. J., W. A. Link, J. D. Nichols, G. L. Hadley, R. A. Garrott, and K. M. Proffitt 2009. An evaluation of density-dependent and density-independent influences on population growth rates in Weddell seals. Ecology 90:975-984.
66. Rotella, J. J., W. A. Link, T. Chambert, G. E. Stauffer, and R. A. Garrott 2012. Evaluating the demographic buffering hypothesis with vital rates estimated for Weddell seals from 30 years of mark-recapture data. J. Anim. Ecol. 81:162-173.
67. Saggiomo, V., G. C. Carrada, O. Mangoni, M. R. d' Alcalà, and A. Russo 1998. Spatial and temporal variability of size-fractionated biomass and primary production in the Ross Sea (Antarctica) during austral spring and summer. J. Mar. Syst. 17:115-127.
68. Schofield, M., and R. Barker 2011. Full open population capture-recapture models with individual covariates. J. Agric. Biol. Environ. Stat. 16:253-268.
69. Schwagmeyer, P. L., and D. W. Mock 2008. Parental provisioning and offspring fitness: size matters. Anim. Behav. 75:291-298.
70. Service, P. M. 2000. Heterogeneity in individual mortality risk and its importance for evolutionary studies of senescence. Am. Nat. 156:1-13.
71. Siepielski, A. M., J. D. DiBattista, and S. M. Carlson 2009. It's about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12:1261-1276.
72. Siniff, D. B., D. P. DeMaster, R. J. Hofman, and L. L. Eberhardt 1977. An analysis of the dynamics of a weddell seal population. Ecol. Monogr. 47:319-335.
73. Smith, B. R., and D. T. Blumstein 2008. Fitness consequences of personality: a meta-analysis. Behav. Ecol. 19:448-455.
74. Smith, W. O., D. G. Ainley, and R. Cattaneo-Vietti 2007. Trophic interactions within the Ross Sea continental shelf ecosystem. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:95-111.
75. Spiegelhalter, D. J., N. G. Best, B. P. Carlin, and A. Van Der Linde 2002. Bayesian measures of model complexity and fit. J. R. Stat. Soc. Series B (Stat. Methodol.) 64:583-639.
76. Steiner, U. K., S. Tuljapurkar, and S. H. Orzack 2010. Dynamic heterogeneity and life history variability in the kittiwake. J. Anim. Ecol. 79:436-444.
77. Tavecchia, G., T. Coulson, B. J. T. Morgan, J. M. Pemberton, J. C. Pilkington, F. M. D. Gulland, et al. 2005. Predictors of reproductive cost in female Soay sheep. J. Anim. Ecol. 74:201-213.
78. Tuljapurkar, S., U. K. Steiner, and S. H. Orzack 2009. Dynamic heterogeneity in life histories. Ecol. Lett. 12:93-106.
79. Van Noordwijk, A. J. 1989. Reaction norms in genetical ecology. Bioscience 39:453-458.
80. Van Noordwijk, A. J., and G. De Jong 1986. Allocation of resources: their influence on variation in life history tactics. Am. Nat. 128:137-142.
81. Vanpé, C., J. Gaillard, P. Kjellander, A. Mysterud, P. Magnien, D. Delorme, et al. 2007. Antler size provides an honest signal of male phenotypic quality in roe deer. Am. Nat. 169:481-493.
82. Vaupel, J. W., and A. I. Yashin 1985. Heterogeneity's ruses: some surprising effects of selection on population dynamics. Am. Stat. 39:176-185.
83. Vindenes, Y., S. Engen, and B.-E. Saether 2008. Individual heterogeneity in vital parameters and demographic stochasticity. Am. Nat. 171:455-467.
84. Weladji, R., A. Loison, J.-M. Gaillard, Ø. Holand, A. Mysterud, N. Yoccoz, et al. 2008. Heterogeneity in individual quality overrides costs of reproduction in female reindeer. Oecologia 156:237-247.
85. Wheatley, K. E., C. J. A. Bradshaw, L. S. Davis, R. G. Harcourt, and M. A. Hindell 2006. Influence of maternal mass and condition on energy transfer in Weddell seals. J. Anim. Ecol. 75:724-733.
86. Wheatley, K., C. Bradshaw, R. Harcourt, and M. Hindell 2008a. Feast or famine: evidence for mixed capital-income breeding strategies in Weddell seals. Oecologia 155:11-20.
87. Wheatley, K. E., P. D. Nichols, M. A. Hindell, R. G. Harcourt, and C. J. A. Bradshaw 2008b. Differential mobilization of blubber fatty acids in lactating weddell seals: evidence for selective use. Physiol. Biochem. Zool. 81:651-662.
88. Williams, T. M., L. A. Fuiman, M. Horning, and R. W. Davis 2004. The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J. Exp. Biol. 207:973-982.
89. Wilson, A. J., and D. H. Nussey 2010. What is individual quality? An evolutionary perspective. Trends Ecol. Evol. 25:207-214.
90. Zuk, M., R. Thornhill, J. D. Ligon, K. Johnson, S. Austad, S. H. Ligon, et al. 1990. The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am. Nat. 136:459-473.