Skip to main content
SpringerLink
Log in

Recruiting age influences male and female survival and population persistence in a long-lived tropical seabird

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Variation in the age at first reproduction may have important implications for growth and dynamics of populations, but these potential impacts remain virtually unexplored. By using 26 years of data from a marked colony of blue-footed boobies Sula nebouxii (Milne-Edwards), we tested whether survival of early recruits is lower in comparison to late recruits, and investigate how different recruiting ages contribute to the persistence of the population. In addition, we simulated changes in the age at recruitment and estimated their impact on population fitness. Our analyses of 1310 capture–recapture histories revealed that the younger males and females initiated reproduction within the first 6 years of life, the lower were their mean annual survival probabilities. Survival did not differ between the sexes and the impact of recruiting age on survival was similar for males and females. Each additional year that male and female boobies delayed the start of reproduction meant an increase of roughly 2 % in their annual survival rates. Male and female recruits 2–5 years old contributed the same to the rate of population growth (λ) regardless of their particular age, but the contribution to population growth started to decline from age 6 years. According to our simulations, delaying reproduction beyond 5 years in the case of females, and beyond 6 years in the case of males, would negatively affect this booby population. Therefore, we suggest that there is selection against recruiting beyond 5–6 years old. This study adds to the nascent empirical literature on long-term fitness consequences of variation in the age at first reproduction in long-lived species, and provides insights into evolution of early and late reproduction and trade-offs from a demographic perspective.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akaike H (1998) Information theory and an extension of the Maximum Likelihood Principle. In: Parzen E, Tanabe K, Kitagawa G (eds) Selected Papers of Hirotugu Akaike SE-15. Springer, New York, pp 199–213

    Chapter  Google Scholar 

  • Amstrup SC, McDonald TL, Manly BFJ (2005) Handbook of Capture-Recapture Analysis. Princeton University Press, New Jersey

    Google Scholar 

  • Ancona S, Drummond H (2013) Life history plasticity of a tropical seabird in response to El Niño anomalies during early life. PLoS One 8:e72665. doi:10.1371/journal.pone.0072665

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ancona S, Sánchez-Colón S, Rodríguez C, Drummond H (2011) El Niño in the Warm Tropics: local sea temperature predicts breeding parameters and growth of blue-footed boobies. J Anim Ecol 80:799–808. doi:10.1111/j.1365-2656.2011.01821.x

    Article  PubMed  Google Scholar 

  • Aubry LM, Koons DN, Monnat J-Y, Cam E (2009) Consequences of recruitment decisions and heterogeneity on age-specific breeding success in a long-lived seabird. Ecology 90:2491–2502

    Article  PubMed  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. doi:10.1086/650726

    Article  PubMed  Google Scholar 

  • Becker PH, Bradley JS (2007) The role of intrinsic factors for the recruitment process in long-lived birds. J Ornithol 148:377–384. doi:10.1007/s10336-007-0157-x

    Article  Google Scholar 

  • Benton TG, Grant A (1999) Elasticity analysis as an important tool in evolutionary and population ecology. Trends Ecol Evol 14:467–471. doi:10.1016/S0169-5347(99)01724-3

    Article  PubMed  Google Scholar 

  • Benton TG, Grant A (2000) Evolutionary fitness in ecology: comparing measures of fitness in stochastic, density-dependent environments. Evol Ecol Res 2:769–789

    Google Scholar 

  • Blomquist GE (2009) Trade-off between age of first reproduction and survival in a female primate. Biol Lett 5:339–342

    Article  PubMed Central  PubMed  Google Scholar 

  • Brommer JE, Merilä J, Kokko H (2002) Reproductive timing and individual fitness. Ecol Lett 5:802–810. doi:10.1046/j.1461-0248.2002.00369.x

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • 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 Central  CAS  PubMed  Google Scholar 

  • Charnov EL (1990) On evolution of age of maturity and the adult lifespan. J Evol Biol 3:139–144

    Article  Google Scholar 

  • Clobert J (1995) Capture–recapture and evolutionary ecology: a difficult wedding? J Appl Stat 22:989–1008. doi:10.1080/02664769524757

    Article  Google Scholar 

  • Clutton-Brock TH, Huchard E (2013) Social competition and selection in males and females. Philos Trans R Soc B Biol Sci 368:20130074

    Article  CAS  Google Scholar 

  • Cole LC (1954) The population consequences of life history phenomena. Q Rev Biol 29:103–137

  • Cox R, Calsbeek R (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173:176–187. doi:10.1086/595841

    Article  PubMed  Google Scholar 

  • Crone EE, Menges ES, Ellis MM et al (2011) How do plant ecologists use matrix population models? Ecol Lett 14:1–8. doi:10.1111/j.1461-0248.2010.01540.x

    Article  PubMed  Google Scholar 

  • De Kroon H, Plaisier A, van Groenendael J, Caswell H (1986) Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67:1427–1431

    Article  Google Scholar 

  • De Kroon H, Van Groenendael J, Ehrlén J (2000) Elasticities: a review of methods and model limitations. Ecology 81:607–618

    Article  Google Scholar 

  • Doherty P, White G, Burnham K (2012) Comparison of model building and selection strategies. J Ornithol 152:317–323. doi:10.1007/s10336-010-0598-5

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol I0:374–378

    Article  Google Scholar 

  • Gibbons JW, Lovich JE (1990) Sexual dimorphism in turtles with emphasis on the slider turtle (Trachemys scripta). Herpetol Monogr 4:1–29

    Article  Google Scholar 

  • Green WCH, Rothstein A (1991) Trade-offs between growth and reproduction in female bison. Oecologia 86:521–527. doi:10.1007/BF00318318

    Article  Google Scholar 

  • Gude JA, Cunningham JA, Herbert JT, Baumeister T (2012) Deer and elk hunter recruitment, retention, and participation trends in Montana. J Wildl Manag 76:471–479. doi:10.1002/jwmg.272

    Article  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 

  • Houston AI, McNamara JM (1999) Models of adaptive behaviour: an approach based on state. Cambridge University Press, Cambridge

    Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. doi:10.1016/j.tree.2003.10.013

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233–238

    Article  CAS  PubMed  Google Scholar 

  • Krüger O (2005) Age at first breeding and fitness in goshawk Accipiter gentilis. J Anim Ecol 74:266–273. doi:10.1111/j.1365-2656.2004.00920.x

    Article  Google Scholar 

  • Krüger O, Lindström J (2001) Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography. Oikos 93:260–273. doi:10.1034/j.1600-0706.2001.930209.x

    Article  Google Scholar 

  • Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  • Legendre S (2004) Age structure, mating system, and population viability. In: Ferriére R, Dieckmann U, Couvet D (eds) Evolutionary conservation biology. Cambridge University Press, Cambridge, pp 41–58

    Chapter  Google Scholar 

  • Leslie PH (1945) On the use of matrices in certain population mathematics. Biometrika 33:183–212

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

    Article  PubMed  Google Scholar 

  • Macip-Ríos R, Brauer-Robleda P, Zúñiga-Vega JJ, Casas-Andreu G (2011) Demography of two populations of the Mexican mud turtle (Kinosternon integrum) in central Mexico. Herpetol J 21:235–245

    Google Scholar 

  • Maklakov AA, Kremer N, Arnqvist G (2007) The effects of age at mating on female life-history traits in a seed beetle. Behav Ecol 18:551–555. doi:10.1093/beheco/arm016

    Article  Google Scholar 

  • McAdam AG, Boutin S, Sykes AK, Humphries MM (2007) Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Ecoscience 14:362–369

    Article  Google Scholar 

  • McGraw JB, Caswell H (1996) Estimation of individual fitness from life-history data. Am Nat 147:47–64

  • Metcalf CJE, Pavard S (2007) Why evolutionary biologists should be demographers. Trends Ecol Evol 22:205–212. doi:10.1016/j.tree.2006.12.001

    Article  PubMed  Google Scholar 

  • Mukhopadhyay A, Tissenbaum HA (2007) Reproduction and longevity: secrets revealed by C. elegans. Trends Cell Biol 17:65–71

    Article  CAS  PubMed  Google Scholar 

  • Murray BG (1997) Population dynamics of evolutionary change: demographic parameters as indicators of fitness. Theor Popul Biol 51:180–184. doi:10.1006/tpbi.1997.1313

    Article  PubMed  Google Scholar 

  • Nelson B (2005) Pelicans, cormorants, and their relatives: Pelecanidae, Sulidae, Phalacrocoracidae, Anhingidae, Fregatidae, Phaethontidae. Oxford University Press, Oxford

    Google Scholar 

  • Nussey DH, Kruuk LEB, Donald A et al (2006) The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol Lett 9:1342–1350. doi:10.1111/j.1461-0248.2006.00989.x

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Peña B (2009) Variación de la fecha de puesta del bobo de patas azules. B.Sc. Thesis. Universidad Nacional Autónoma de México

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

    Article  Google Scholar 

  • Ramos AG, Nunziata SO, Lance SL et al (2014) Habitat structure and colony structure constrain extrapair paternity in a colonial bird. Anim Behav 95:121–127. doi:10.1016/j.anbehav.2014.07.003

    Article  Google Scholar 

  • Roff DA (2002) Life History Evolution. Sinauer Associates, Incorporated, Sunderland

    Google Scholar 

  • Sæther B-E, Coulson T, Grøtan V et al (2013) How life history influences population dynamics in fluctuating environments. Am Nat 182:743–759. doi:10.1086/673497

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Velando A, Drummond H, Torres R (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc Biol Sci 273:1443–1448. doi:10.1098/rspb.2006.3480

    Article  PubMed Central  PubMed  Google Scholar 

  • Velando A, Drummond H, Torres R (2010) Senescing sexual ornaments recover after a sabbatical. Biol Lett 6:194–196

    Article  PubMed Central  PubMed  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139. doi:10.1080/00063659909477239

    Article  Google Scholar 

  • Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214. doi:10.1016/j.tree.2009.10.002

    Article  PubMed  Google Scholar 

  • Zhang H, Rebke M, Becker PH, Bouwhuis S (2014) Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird. J Anim Ecol. doi:10.1111/1365-2656.12259

    Google Scholar 

Download references

Acknowledgments

J.L. Osorno, R. Torres and numerous volunteers provided valuable help in the field and on the database. Logistical support and permissions to work on Isla Isabel were provided by the Secretaría de Marina, Armada de México and Secretaría de Medio Ambiente y Recursos Naturales (Comisión Nacional de Áreas Naturales Protegidas and staff of the Parque Nacional Isla Isabel). We are very grateful to numerous fishermen of Nayarit and Sinaloa for their friendship and valuable support in the field and to G. Madrid (APPIO) for his technical support during data processing. Funds were provided by Universidad Nacional Autónoma de México (UNAM), the Consejo Nacional de Ciencia y Tecnología (CONACYT, 81823, 47599, 34500-V, 4722-N9407, D112-903581, PCCNCNA-031528, 31973H and 104313) and the National Geographic Society. S. Ancona was supported by a Postdoctoral Grant provided by the Dirección General de Asuntos del Personal Académico—UNAM (Programa de Becas Posdoctorales en la UNAM 2013).

Author information

Authors and Affiliations

  1. Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, México, D.F., Mexico

    Sergio Ancona & J. Jaime Zúñiga-Vega

  2. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Mexico, D.F., Mexico

    Cristina Rodríguez & Hugh Drummond

  3. Department of Biology and Biochemistry, University of Bath, Bath, BA2 7AY, UK

    María Cristina Carmona-Isunza

Authors
  1. Sergio Ancona
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Jaime Zúñiga-Vega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristina Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Cristina Carmona-Isunza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hugh Drummond
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergio Ancona.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Model-averaged resighting probabilities (p) from Cormack–Jolly–Seber models fitted to capture–recapture histories of 10,850 blue-footed booby fledglings that were ringed and subsequently resighted as breeders every year during April–May on Isla Isabel, from 1988 to 2013. Different sources of variation for p, including effects of time (year), sex, age (23 age classes), and their interactions were tested. The parameterization for p with strongest support in the capture–recapture dataset was time-varying p for all individuals 3 years and older (with no differences among all these adult age classes), with constant p for fledglings and 1- and 2-year-old individuals. Hence, all subsequent models that examined variation in survival probabilities were fitted to data using this parameterization for p. (TIFF 156733 kb)

Fig. S2

11-year lifespan (i.e., the age at the last observed breeding record in the 11 seasons following the natal year) of 2315 recruits that fledged between 1988 and 2002 (13 cohorts; no fledglings were banded in 1990, and no chicks fledged in 1992 due to a severe El Niño conditions) and bred for the first time at age 2–6 years. This pattern is consistent with the model with strongest support in the mark-recapture data showing that lower apparent annual survival is predicted by younger recruitment. (TIFF 158503 kb)

Supplementary material 3 (DOCX 15 kb)

Supplementary material 4 (DOCX 17 kb)

Supplementary material 5 (DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ancona, S., Jaime Zúñiga-Vega, J., Rodríguez, C. et al. Recruiting age influences male and female survival and population persistence in a long-lived tropical seabird. Evol Ecol 29, 799–812 (2015). https://doi.org/10.1007/s10682-015-9781-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-015-9781-8

Keywords

Search

Navigation