Skip to main content
Log in

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird

  • Population ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Niño event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahnesjö I, Kvarnemo C, Merilaita S (2001) Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behav Ecol 12:397–401

    Article  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Chastel O, Sorci G (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60:1913–1924

    PubMed  Google Scholar 

  • Anderson DJ (1989) Differential responses of boobies and other seabirds in the Galápagos to the 1986–87 El Niño Southern Oscillation event. Mar Ecol Prog Ser 52:209–216

    Article  Google Scholar 

  • Anderson DJ, Ricklefs RE (1992) Brood size and food provisioning in masked and blue-footed boobies (Sula spp.). Ecology 73:1363–1374

    Article  Google Scholar 

  • Beamonte-Barrientos R, Velando A, Drummond H, Torres R (2010) Senescence of maternal effects: aging influences egg quality and rearing capacities of a long-lived bird. Am Nat 175:469–480

    Article  PubMed  Google Scholar 

  • Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581

    PubMed  CAS  Google Scholar 

  • Blondel J, Pradel R, Lebreton J-D (1992) Low fecundity insular blue tits do not survive better as adults than high fecundity mainland ones. J Anim Ecol 61:205–213

    Article  Google Scholar 

  • Bonduriansky R, Maklakov A, Zajitschek F, Brooks R (2008) Sexual selection, sexual conflict and the evolution of ageing and life span. Funct Ecol 22:443–453

    Article  Google Scholar 

  • Boulinier T, Sorci G, Clobert J, Danchin E (1997) An experimental study of the costs of reproduction in the kittiwake Rissa tridactyla: comment. Ecology 78:1284–1287

    Google Scholar 

  • Cam E, Link WA, Cooch EG, Monnat J-Y, Danchin E (2002) Individual covariation in life-history traits: seeing the trees despite the forest. Am Nat 159:96–105

    Article  PubMed  Google Scholar 

  • Castillo-Alvarez A, Chavez-Peón A (1983) Ecología reproductiva e influencia del comportamiento en el control del número de crias en el bobo de patas azules, Sula nebouxii, en la Isla Isabel, Nay. BSc Thesis, Universidad Nacional Autonoma de Mexico, Mexico

  • Charmantier A, Perrins C, McCleery RH, Sheldon BC (2006) Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc Natl Acad Sci USA 103:6587–6592

    Article  PubMed  CAS  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Dentressangle F, Boeck L, Torres R (2008) Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 62:1899–1908

    Article  Google Scholar 

  • Descamps S, Boutin S, Berteaux D, Gaillard J-M (2008) Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117:1406–1416

    Article  Google Scholar 

  • Drummond H, Osorno JL, García C, Torres R, Merchant H (1991) Sexual dimorphism and sibling competition: implications for avian sex ratios. Am Nat 138:623–641

    Article  Google Scholar 

  • Drummond H, Torres R, Krishnan VV (2003) Buffered development: resilience after aggressive subordination in infancy. Am Nat 161:794–807

    Article  PubMed  Google Scholar 

  • Evans RM (1990) The relationship between parental input and investment. Anim Behav 39:797–798

    Article  Google Scholar 

  • Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol 209:2377–2383

    Article  PubMed  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds-hypotheses and tests. Trends Ecol Evol 10:374–378

    Article  PubMed  CAS  Google Scholar 

  • Guerra M, Drummond H (1995) Reversed sexual size dimorphism and parental care: minimal division of labour in the blue-footed booby. Behaviour 132:479–496

    Article  Google Scholar 

  • Gustafsson L, Pärt T (1990) Acceleration of senescence in the collared flycatcher Ficadula albicollis by reproductive costs. Nature 347:279–281

    Article  Google Scholar 

  • Hadley GL, Rotella JJ, Garrott RA (2007) Evaluation of reproductive costs for weddell seals in Erebus Bay, Antarctica. J Anim Ecol 76:448–458

    Article  PubMed  Google Scholar 

  • Kim S-Y, Torres R, Rodríguez C, Drummond H (2007a) Effects of breeding success, mate fidelity and senescence on breeding dispersal of male and female blue-footed boobies. J Anim Ecol 76:471–479

    Article  PubMed  Google Scholar 

  • Kim S-Y, Torres R, Domínguez CA, Drummond H (2007b) Lifetime philopatry in the blue-footed booby: a longitudinal study. Behav Ecol 18:1132–1138

    Article  Google Scholar 

  • Kim S-Y, Drummond H, Torres R, Velando A (2011) Evolvability of an avian life-history trait declines with father’s age. J Evol Biol 24:295–302

    Google Scholar 

  • Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304

    Article  PubMed  CAS  Google Scholar 

  • Kirkwood TBL, Rose MR (1991) Evolution of senescence-late survival sacrificed for reproduction. Philos Trans R Soc Lond B 332:15–24

    Article  CAS  Google Scholar 

  • Kruuk LEB, Slate J, Wilson AJ (2008) New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu Rev Ecol Evol Syst 39:525–548

    Article  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  • Medawar PB (1952) An unsolved problem of biology. Lewis, London

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Michener GR, Locklear L (1990) Differential costs of reproductive effort for male and female Richardson’s ground squirrels. Ecology 71:855–868

    Article  Google Scholar 

  • Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc Lond B 265:1731–1735

    Article  Google Scholar 

  • Moyes K, Morgan BJT, Morris A, Morris SJ, Clutton-Brock TH, Coulson T (2009) Exploring individual quality in a wild population of red deer. J Anim Ecol 78:406–413

    Article  PubMed  Google Scholar 

  • Nelson JB (2005) Pelicans Cormorants and their relatives. Oxford University Press, Oxford

    Google Scholar 

  • Newton I (1985) Lifetime reproductive output of female sparrowhawks. J Anim Ecol 54:241–253

    Article  Google Scholar 

  • Nussey DH, Kruuk LEB, Donald A, Fowlie M, Clutton-Brock TH (2006) The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol Lett 9:1342–1350

    Article  PubMed  Google Scholar 

  • Nussey DH, Coulson T, Festa-Bianchet M, Gaillard J-M (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406

    Article  Google Scholar 

  • Oli MK, Hepp GR, Kennamer RA (2002) Fitness consequences of delayed maturity in female wood ducks. Evol Ecol Res 4:563–576

    Google Scholar 

  • Oro D, Torres R, Rodriguez C, Drummond H (2010) Climatic influence on demographic parameters of a tropical seabird varies with age and sex. Ecology 91:1205–1214

    Article  PubMed  Google Scholar 

  • Osorio-Beristain M, Drummond H (1993) Natal dispersal and deferred breeding in the blue-footed booby. Auk 110:234–239

    Google Scholar 

  • Partridge L (1992) Lifetime reproductive success and life-history evolution. In: Newton I (ed) Lifetime reproduction in birds. Academic, London, pp 421–440

    Google Scholar 

  • Partridge L, Farquhar M (1981) Sexual activity reduces lifespan of male fruitflies. Nature 294:580–582

    Article  Google Scholar 

  • Pyle P, Nur N, Sydeman WJ, Emslie SD (1997) Cost of reproduction and the evolution of deferred breeding in the western gull. Behav Ecol 8:140–147

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org

  • Reed ET, Gauthier G, Pradel R, Lebreton J-D (2003) Age and environmental conditions affect recruitment in greater snow geese. Ecology 84:219–230

    Article  Google Scholar 

  • Reed ET, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP (2008) Repoductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. Am Nat 171:E89–E101

    Article  PubMed  Google Scholar 

  • Reid JM, Monaghan P, Ruxton GD (2002) Males matter: the occurrence and consequences of male incubation in starlings (Sturnus vulgaris). Behav Ecol Sociobiol 51:255–261

    Article  Google Scholar 

  • Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2003) Age-specific reproductive performance in red-billed choughs Pyrrhocorax pyrrhocorax: patterns and processes in a natural population. J Anim Ecol 72:765–776

    Article  Google Scholar 

  • Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425

    Article  PubMed  Google Scholar 

  • Rice WR, Chippindale AK (2001) Intersexual ontogenetic conflict. J Evol Biol 14:685–693

    Article  Google Scholar 

  • Roff DA (2002) Life history evolution. Sinauer, Sunderland

    Google Scholar 

  • SAS Institute (1999) SAS/STAT, version 8. SAS Institute, Cary

    Google Scholar 

  • Schaffer WM (1974) Selection for optimal life histories: the effects of age structure. Ecology 55:291–303

    Article  Google Scholar 

  • Sedinger JS, Flint PL, Lindberg MS (1995) Environmental influence on life-history traits: growth, survival, and fecundity in black brant (Branta bernicla). Ecology 76:2404–2414

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Tavecchia G, Pradel R, Boy V, Johnson AR, Cézilly F (2001) Sex- and age-related variation in survival and cost of first reproduction in greater flamingos. Ecology 82:165–174

    Article  Google Scholar 

  • Torres R, Drummond H (1999) Variably male-biased sex ratio in a marine bird with females larger than males. Oecologia 118:16–22

    Article  PubMed  CAS  Google Scholar 

  • van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am Nat 167:764–771

    Google Scholar 

  • van de Pol M, Wright J (2009) A simple method for distinguishing within versus between-subject effects using mixed models. Anim Behav 77:753–758

    Article  Google Scholar 

  • van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influences on variation in life history tactics. Am Nat 128:137–142

    Article  Google Scholar 

  • Velando A, Alonso-Alvarez C (2003) Differential body condition regulation by males and females in response to experimental manipulations of brood size and parental effort in the blue-footed booby. J Anim Ecol 72:846–856

    Article  Google Scholar 

  • Velando A, Drummond H, Torres R (2006a) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc Lond B 273:1443–1448

    Article  Google Scholar 

  • Velando A, Beamonte-Barrientos R, Torres R (2006b) Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment. Oecologia 149:535–542

    Article  PubMed  Google Scholar 

  • Viallefont A, Cooch EG, Cooke F (1995) Estimation of trade-offs with capture-recapture models: a case study on the lesser snow goose. J Appl Stat 22:847–861

    Article  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411

    Article  Google Scholar 

Download references

Acknowledgments

We thank P. Monaghan and N. Metcalfe for very helpful comments on an earlier manuscript, J. Stamps for references and discussion, and C. Rodríguez, J. L. Osorno and numerous volunteers and students for dedicated work in the field and on the database. Annual fieldwork on Isla Isabel depended on the generous support of many fishermen, the Mexican Secretaría del Medioambiente y Recursos Naturales and the Mexican navy. Finance was provided by the Mexican Consejo Nacional de Ciencia y Tecnología (4722-N9407, C01-47599, D112-903581, PCCNCNA-031528), the Universidad Nacional Autónoma de México (IN211491), the National Geographic Society (3065-85, 4535-91), and the Conservation and Research Foundation. S.-Y. Kim was supported by a postdoctoral fellowship of the UNAM and by the Spanish Ministerio de Ciencia y Tecnología (CGL2006-10357-C02-01/BOS) and the Xunta de Galicia (Isidro Parga Pondal fellowship). The field procedures we performed did not involve any licensed procedures and complied with the current laws of Mexico.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sin-Yeon Kim.

Additional information

Communicated by Christopher Johnson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, SY., Velando, A., Torres, R. et al. Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird. Oecologia 166, 615–626 (2011). https://doi.org/10.1007/s00442-011-1914-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-1914-3

Keywords

Navigation