Skip to main content
Log in

Either taking it easy or feeling too tired: old Cory’s Shearwaters display reduced activity levels while at sea

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

It has long been known that birds change their behaviour, reproductive performance and survival as they mature, including in the first few years after recruitment into the breeding population. However, and contrasting with the description of patterns of actuarial and reproductive senescence in later years, there are surprisingly few studies documenting changes in behaviour in old individuals. Such studies are important, as birds provide particularly interesting models for studying the biology of senescence. It has been suggested that, unlike mammals, birds may remain physically fit until an advanced age, yet this has limited empirical support. In this paper, we used activity (immersion) loggers to show that old (>26 years) Cory’s Shearwaters Calonectris diomedea are less active when foraging at sea, spend more time resting on the water and have a smaller number of take-offs and landings during darkness, when compared to experienced mid-aged individuals (13–20 years old). Old individuals also tended to have reduced immune response against an experimental challenge using phytohaemagglutinin. These results are in line with observed reductions in activity levels with age in a wide range of non-avian taxa, and may suggest that old seabirds are physically less fit than younger individuals. Alternatively, old birds might simply be more experienced and their reduction in activity might reflect a strategic regulation of investment in different activities. Our study illustrates the potential for gaining insights into avian aging patterns and processes by looking into the behaviour of model organisms. We therefore encourage more research focusing on behavioural parameters that may reflect variations in physical condition or strategic choices, during both the breeding and non-breeding seasons.

Zusammenfassung

Es ist bereits seit längerem bekannt, dass sich das Verhalten, der Bruterfolg und die Überlebensrate von Vögeln mit zunehmendem Alter verändert. Trotz der Beschreibung solcher Muster von Sterblichkeitsund reproduktiver Vergreisung in späteren Jahren gibt es erstaunlich wenige Studien, die eine derartige Veränderung im Verhalten alter Individuen dokumentieren. Solche Studien sind wichtig, weil Vögel ein besonders interessantes Modellsystem für die Untersuchung der Biologie von Vergreisung darstellen. Anders als bei Säugetieren wurde vorgeschlagen, dass Vögel bis ins hohe Alter physisch gesund bleiben. Dies wird jedoch nur im begrenzten Maße von empirischen Daten unterstützt. In der vorliegenden Studie verwendeten wir Aktivitätslogger, um zu zeigen, dass 26-jährige Gelbschnabel-Sturmtaucher Calonectris diomedea weniger aktiv sind, während sie auf See furagieren. Sie haben kürzere Ruhepausen auf dem Wasser und eine geringere Anzahl Starts und Landungen während der Dunkelheit, im Vergleich mit erfahrenen mittel alten Individuen (13–20 Jahre alt). Alte Individuen neigten auch zu einer reduzierten Immunreaktion auf eine experimentelle Injektion von Phytohaemagglutinin. Diese Ergebnisse stimmen im Wesentlichen überein mit der beobachteten Abnahme von Aktivität mit zunehmendem Alter in einer großen Anzahl anderer Tiergruppen. Es kann sein, dass alte Seevögel physisch weniger fit sind als jüngere. Alternativ könnten ältere Vögel auch erfahrener sein, und die Aktivitätsreduktion könnte eine strategische Regulierung der Allokation von Investment in unterschiedliche Aktivitäten sein. Unsere Untersuchung zeigt, dass detaillierte Studien des Verhaltens von Modellorganismen das Potential haben, Muster und Alterungsprozesse bei Vögeln zu erklären. Wir regen deshalb mehr Verhaltensstudien an, die die Variation in der physischer Kondition oder verschiedene strategischen Entscheidungen reflektieren, und dies sowohl in wie außerhalb der Brutsaison.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, Oxford

    Google Scholar 

  • Bevan RM, Butler PJ, Woakes AJ, Prince PA (1995) The energy expenditure of free-ranging black-browed albatrosses. Philos Trans R Soc Lond B 350:119–131

    Google Scholar 

  • Carter CS, Sonntag WE, Onder WE, Pahor M (2002) Physical performance and longevity in aged rats. J Gerontol 57:B193–B197

    Google Scholar 

  • Catry P, Phillips RA, Phalan B, Silk JRD, Croxall JP (2004) Foraging strategies of grey-headed albatrosses Thalassarche chrysostoma: integration of movements, activity and feeding events. Mar Ecol Progr Ser 280:261–273

    Google Scholar 

  • Catry P, Phillips RA, Phalan B, Croxall JP (2006) Senescence effects in an extremely long-lived bird: the grey-headed albatross Thalassarche chrysostoma. Proc R Soc Lond B 273:1625–1630

    Google Scholar 

  • Coulson JC, Fairweather JA (2001) Reduced reproductive performance prior to death in the black-legged kittiwake: senescence or terminal illness? J Avian Biol 32:146–152

    Google Scholar 

  • Edwards AM, Phillips RA, Watkins NW, Freeman MP, Murphy EJ, Afanasyev V, Buldyrev SV, da Luz MGE, Raposo EP, Stanley HE, Viswanathan GM (2007) Overturning evidence of Levy flight searches by wandering albatrosses, bumblebees and deer. Nature 449:1044–1049

    CAS  PubMed  Google Scholar 

  • Emborg ME, Ma SY, Mufson EJ, Levey AI, Taylor MD, Brown WD, Holden JE, Kordower JH (1998) Age-related declines in nigral neuronal function correlate with motor impairments in rhesus monkeys. J Comp Neurol 401:253–265

    CAS  PubMed  Google Scholar 

  • Fernández JR, Grant MD, Tulli NM, Karkowski LM, McClearn GE (1999) Differences in locomotor activity across the lifespan of Drosophila melanogaster. Exp Gerontol 34:621–631

    PubMed  Google Scholar 

  • Forero MG, González-Solis J, Igual JM, Hobson KA, Ruíz X, Viscor G (2006) Ecological and physiological variance in T-cell mediated immune response in Cory’s shearwaters. Condor 108:865–876

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Granadeiro JP (1993) Variation in measurements of Cory’s Shearwater between populations and sexing by discriminant analysis. Ring Migr 14:103–112

    Google Scholar 

  • Granadeiro JP, Dias MP, Rebelo R, Santos CD, Catry P (2006) Numbers and population trends of Cory’s shearwater Calonectris diomedea at Selvagem Grande, Northeast Atlantic. Waterbirds 29:56–60

    Google Scholar 

  • Hanssen SA (2006) Cost of an immune challenge and terminal investment in a long-lived bird. Ecology 87:2440–2446

    PubMed  Google Scholar 

  • Haussmann MF, Winkler DW, Huntington CE, Vleck D, Sanneman CE, Hanley D, Vleck CM (2005) Cell-mediated immunosenescence in birds. Oecologia 145:270–275

    PubMed  Google Scholar 

  • Hornung OP, Danker-Hopfe H, Heuser I (2005) Age-related changes in sleep and memory: commonalities and interrelationships. Exp Gerontol 40:279–285

    PubMed  Google Scholar 

  • Igual JM, Forero MG, Tavecchia G, González-Solis J, Martínez-Abraín A, Hobson KA, Ruiz X, Oro D (2005) Short-term effects of data-loggers on Cory’s shearwaters Calonectris diomedea. Mar Biol 146:619–624

    Google Scholar 

  • Ingram DK (2000) Age-related decline in physical activity: generalization to nonhumans. Med Sci Sports Exerc 32:1623–1629

    CAS  PubMed  Google Scholar 

  • Jones OR et al (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol Lett 11:664–673

    PubMed  Google Scholar 

  • Kennedy MW, Nager MG (2006) The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol 21:653–655

    PubMed  Google Scholar 

  • Lecomte VJ, Sorci G, Cornet S, Jaeger A, Faivre B, Arnoux E, Gaillard M, Trouvé C, Besson D, Chastel O, Weimerskirch H (2010) Patterns of aging in the long-lived wandering albatross. Proc Natl Acad Sci USA 107:6370–6375

    CAS  PubMed  PubMed Central  Google Scholar 

  • MacNulty DR, Smith DW, Vucetich JA, Mech LD, Stahler DR, Packer C (2009) Predatory senescence in ageing wolves. Ecol Lett 12:1347–1356

    PubMed  Google Scholar 

  • McNamara JM, Houston AI, Barta Z, Scheuerlein A, Fromhage L (2009) Deterioration, death and the evolution of reproductive restraint in late life. Proc R Soc Lond B 276:4061–4066

    Google Scholar 

  • Mougin J-L (2002) Influence de la sénilité sur la réussite de la reproduction chez le puffin cendré Calonectris diomedea. Bol Mus Mun Funchal 53:27–34

    Google Scholar 

  • Mougin J-L, Jouanin C, Roux F (2000) Démographie du puffin cendré Calonectris diomedea de Selvagem Grande. Rev Ecol (Terre Vie) 55:275–290

    Google Scholar 

  • Némoz-Bertholet F, Aujard F (2003) Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Exp Gerontol 38:407–414

    PubMed  Google Scholar 

  • Newton I (ed) (1989) Lifetime reproduction in birds. Academic, London

    Google Scholar 

  • Nisbet ICT (2001) Detecting and measuring senescence in wild birds: experience with long-lived seabirds. Exp Gerontol 36:833–843

    CAS  PubMed  Google Scholar 

  • Paredes SD, Terrón MP, Cubero J, Valero V, Barriga C, Reiter RJ, Rodríguez AB (2006) Comparative study of the activity/rest rhythms in young and old ringdove (Streptopelia risoria): correlation with serum levels of melatonin and serotonin. Chronobiol Int 23:779–793

    CAS  PubMed  Google Scholar 

  • Passos C, Navarro J, Giudici A, González-Solís J (2010) Effects of extra mass on the pelagic behavior of a seabird. Auk 127:100–107

    Google Scholar 

  • Phalan B, Phillips RA, Silk JRD, Afanasyev V, Fukuda A, Fox J, Catry P, Higuchi H, Croxall JP (2007) Foraging behaviour of four albatross species by night and day. Mar Ecol Progr Ser 340:271–286

    Google Scholar 

  • Ricklefs RE (2000) Intrinsic aging-related mortality in birds. J Avian Biol 31:103–111

    Google Scholar 

  • Ricklefs RE (2008) The evolution of senescence from a comparative perspective. Funct Ecol 22:379–392

    Google Scholar 

  • Ropert-Coudert Y, Wilson RP (2005) Trends and perspectives in animal-attached remote sensing. Front Ecol Environ 3:437–444

    Google Scholar 

  • Sallis JF (2000) Age-related decline in physical activity: a synthesis of human and animal studies. Med Sci Sports Exerc 32:1598–1600

    CAS  PubMed  Google Scholar 

  • Sergio F, Blas J, Hiraldo F (2009) Predictors of floater status in a long-lived bird: a cross-sectional and longitudinal test of hypotheses. J Anim Ecol 78:109–118

    PubMed  Google Scholar 

  • Shaffer SA, Costa DP, Weimerskirch H (2001) Behavioural factors affecting foraging effort of breeding wandering albatross. J Anim Ecol 70:864–874

    Google Scholar 

  • Siwak CT, Murphey HL, Muggenburg BA, Milgram NW (2002) Age-dependent decline in locomotor activity in dogs is environment specific. Physiol Behav 75:65–70

    CAS  PubMed  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Google Scholar 

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

    Google Scholar 

  • Thibault J-C, Bretagnolle V, Rabouam C (1997) Calonectris diomedea Cory’s shearwater. BWP Update 1:75–98

    Google Scholar 

  • Thorup K, Alerstam T, Hake M, Kjellén M (2003) Bird orientation: compensation for wind drift in migrating raptors is age dependent. Proc R Soc Lond B (Suppl.) 270:S8–S11

    Google Scholar 

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

    Google Scholar 

  • Vleck CM, Haussmann ME, Vleck D (2007) Avian senescence: underlying mechanisms. J Ornithol 148:S611–S624

    Google Scholar 

  • Weimerskirch H, Guionnet T, Martin J, Shaffer SA, Costa DP (2000) Fast and fuel efficient? Optimal use of wind by flying albatrosses. Proc R Soc Lond B 267:1869–1874

    CAS  Google Scholar 

  • Wooller RD, Bradley JS, Croxall JP (1992) Long-term population studies of seabirds. Trends Ecol Evol 7:111–114

    CAS  PubMed  Google Scholar 

  • Wunderle JM (1991) Age-specific foraging proficiency in birds. Curr Ornithol 8:273–324

    Google Scholar 

  • Yamamoto T, Takahashi A, Yoda K, Katsumata N, Watanabe S, Sato K, Trathan PN (2008) The lunar cycle affects at-sea behaviour in a pelagic seabird, the streaked shearwater Calonectris leucomelas. Anim Behav 76:1647–1652

    Google Scholar 

Download references

Acknowledgments

Parque Natural da Madeira, and particularly Dília Menezes provided permissions to carry out the work and, together with the wardens at the Nature Reserve where this study took place, gave important logistical support. Hany Alonso, Rafael Matias, Maria Dias, Miguel Lecoq, Rui Rebelo, Filipe Moniz, Ana Leal, Ricardo Martins and others helped with fieldwork. The manuscript benefited from the comments of two anonymous referees. This study is an output from a project on the ecology and senescence in Cory’s Shearwaters (PDCT/MAR/58778/2004) supported by Fundação para a Ciência e a Tecnologia (FCT—Portugal) and FEDER. P. Catry benefited from postdoctoral fellowships from FCT (BPD/11631/02 and SFRH/BPD/30031/2006) and further support was received through Programa Plurianual (UI&D 331/94).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paulo Catry.

Additional information

Communicated by P. H. Becker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Catry, P., Granadeiro, J.P., Ramos, J. et al. Either taking it easy or feeling too tired: old Cory’s Shearwaters display reduced activity levels while at sea. J Ornithol 152, 549–555 (2011). https://doi.org/10.1007/s10336-010-0616-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-010-0616-7

Keywords

Navigation