Skip to main content

Costs of reproduction and carry-over effects in breeding albatrosses

  • Glenn T. Crossin (a1), richard A. Phillips (a2), Christine R. Lattin (a3), L. Michael Romero (a3), Xavier Bordeleau (a1), Christopher M. Harris (a4), Oliver P. Love (a4) and Tony D. Williams (a5)...

We investigated the physiology of two closely related albatross species relative to their breeding strategy: black-browed albatrosses (Thalassarche melanophris) breed annually, while grey-headed albatrosses (T. chrysostoma) breed biennially. From observations of breeding fate and blood samples collected at the end of breeding in one season and feather corticosterone levels (fCort) sampled at the beginning of the next breeding season, we found that in both species some post-breeding physiological parameters differed according to breeding outcome (successful, failed, deferred). Correlations between post-breeding physiology and fCort, and links to future breeding decisions, were examined. In black-browed albatrosses, post-breeding physiology and fCort were not significantly correlated, but fCort independently predicted breeding decision the next year, which we interpret as a possible migratory carry-over effect. In grey-headed albatrosses, post-breeding triglyceride levels were negatively correlated with fCort, but only in females, which we interpret as a potential cost of reproduction. However, this potential cost did not carry-over to future breeding in the grey-headed albatrosses. None of the variables predicted future breeding decisions. We suggest that biennial breeding in the grey-headed albatrosses may have evolved as a strategy to buffer against the apparent susceptibility of females to negative physiological costs of reproduction. Future studies are needed to confirm this.

Corresponding author
Hide All
Bonier, F., Martin, P.R., Moore, I.T. & Wingfield, J.C. 2009. Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution, 24, 634642.
Bortolotti, G.R., Marchant, T.A., Blas, J. & German, T. 2008. Corticosterone in feathers is a long-term integrated measure of avian stress physiology. Functional Ecology, 22, 494500.
Bugoni, L., Naves, L.C. & Furness, R.W. 2015. Moult of three Tristan da Cunha seabird species sampled at sea. Antarctic Science, 27, 239251.
Catry, P., Poisbleau, M., Lecoq, M. & Phillips, R.A. 2013. Differences in the timing and extent of annual moult of black-browed albatrosses Thalassarche melanophris living in contrasting environments. Polar Biology, 36, 837842.
Crossin, G.T., Cooke, S.J., Goldbogen, J.A. & Phillips, R.A. 2014. Tracking fitness in marine vertebrates: current knowledge and opportunities for future research. Marine Ecology Progress Series, 496, 117.
Crossin, G.T., Love, O.P., Cooke, S.J. & Williams, T.D. 2016. Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context, and reproductive state. Functional Ecology, 30, 116125.
Crossin, G.T., Phillips, R.A., Wynne-Edwards, K.A. & Williams, T.D. 2013a. Postmigratory body condition and ovarian steroid production predict breeding decisions by female gray-headed albatrosses. Physiological and Biochemical Zoology, 86, 761768.
Crossin, G.T., Phillips, R.A., Lattin, C.R., Romero, L.M. & Williams, T.D. 2013b. Corticosterone mediated costs of reproduction link current to future breeding. General and Comparative Endocrinology, 193, 112120.
Crossin, G.T., Phillips, R.A., Trathan, P.N., Fox, D.S., Dawson, A., Wynne-Edwards, K.E. & Williams, T.D. 2012. Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses. General and Comparative Endocrinology, 176, 151157.
Croxall, J.P., Prince, P.A., Rothery, P. & Wood, A.G. 1998. Population changes in albatrosses at South Georgia. In Robertson, G. & Gales, R., eds. Albatross biology and conservation. Chipping Norton: Beatty and Sons, 6983.
Croxall, J.P., Silk, J.R.D., Phillips, R.A., Afanasyev, V. & Briggs, D.R. 2004. Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science, 307, 249250.
Daan, S., Deerenberg, C. & Dijkstra, C. 1996. Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology, 65, 539544.
Descamps, S., Bêty, J., Love, O.P. & Gilchrist, H.G. 2011. Individual optimization of reproduction in a long-lived migratory bird: a test of the condition-dependent model of laying date and clutch size. Functional Ecology, 25, 671681.
Ebbinge, B.S. & Spaans, B. 1995. The importance of body reserves accumulated in spring staging areas in the temperate zone for breeding in dark-bellied brent geese Branta b. bernicla in the high Arctic. Journal of Avian Biology, 26, 105113.
Fairhurst, G.D., Bond, A.L., Hobson, K.A. & Ronconi, R.A. 2015. Feather-based measures of stable isotopes and corticosterone reveal a relationship between trophic position and physiology in a pelagic seabird over a 153-year period. Ibis, 157, 273283.
Guglielmo, C.G. & Williams, T.D. 2003. Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the western sandpiper (Calidris mauri). Physiological and Biochemical Zoology, 76, 8498.
Harms, N.J., Legagneux, P., Gilchrist, H.G., Bêty, J., Love, O.P., Forbes, M.R., Bortolotti, G.R. & Soos, C. 2015. Feather corticosterone reveals effect of moulting condition in the autumn on subsequent reproductive output and survival in an Arctic migratory bird. Proceedings of the Royal Society of London, B282, 10.1098/rspb.2014.2085.
Harrison, X.A., Blount, J.D., Inger, R., Norris, D.R. & Bearhop, S. 2011. Carry-over effects as drivers of fitness differences in animals. Journal of Animal Ecology, 80, 418.
Hector, J.A.L., Follett, B.K. & Prince, P.A. 1986. Reproductive endocrinology of the black-browed albatross Diomedea melanophris and the grey-headed albatross Diomedea chrysostoma . Journal of Zoology, 208, 237253.
Hennin, H.L., Legagneux, P., Bêty, J., Williams, T.D., Gilchrist, H.G., Baker, T.M. & Love, O.P. 2015. Pre-breeding energetic management in a mixed-strategy breeder. Oecologia, 177, 235243.
Jouventin, P. & Dobson, F.S. 2002. Why breed every other year? The case of albatrosses. Proceedings of the Royal Society of London, B269, 19551961.
Kalmbach, E., Griffiths, R., Crane, J.E. & Furness, R.W. 2004. Effects of experimentally increased egg production on female body condition and laying dates in the great skua Stercorarius skua . Journal of Avian Biology, 35, 501514.
Kouwenberg, A.L., Hipfner, J.M., McKay, D.W. & Storey, A.E. 2013. Corticosterone and stable isotopes in feathers predict egg size in Atlantic puffins Fratercula arctica . Ibis, 155, 413418.
Lattin, C.R., Reed, J.M., DesRochers, D.W. & Romero, L.M. 2011. Elevated corticosterone in feathers correlates with corticosterone-induced decreased feather quality: a validation study. Journal of Avian Biology, 42, 247252.
Love, O.P., Breuner, C.W., Vézina, F. & Williams, T.D. 2004. Mediation of a corticosterone-induced reproductive conflict. Hormones and Behavior, 46, 5965.
Monaghan, P. & Nager, R.G. 1997. Why don’t birds lay more eggs? Trends in Ecology & Evolution, 12, 270272.
Monaghan, P., Bolton, M. & Houston, D.C. 1995. Egg production constraints and the evolution of avian clutch size. Proceedings of the Royal Society of London, B259, 189191.
Monaghan, P., Nager, R.G. & Houston, D.C. 1998. The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proceedings of the Royal Society of London, B265, 17311735.
O’Connor, C.M., Norris, N.R., Crossin, G.T. & Cooke, S.J. 2014. Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere, 5, 10.1890/ES13-00388.1.
Prince, P.A. 1985. Population and energetic aspects of the relationships between black-browed and grey-headed albatrosses and the Southern Ocean marine environment. In Seigfried, W.R., Condy, P.R. & Laws, R.M., eds. Antarctic nutrient cycles and food webs. Berlin: Springer, 473477.
Prince, P.A., Rodwell, S., Jones, M. & Rothery, P. 1993. Molt in black-browed and gray-headed albatrosses Diomedea melanophris and D. chrysostoma . Ibis, 135, 121131.
Phillips, R.A., Silk, J.R.D., Croxall, J.P., Afanasyev, V. & Bennett, V.J. 2005. Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology, 86, 23862396.
Phillips, R.A., Silk, J.R.D., Phalan, B., Catry, P. & Croxall, J.P. 2004. Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proceedings of the Royal Society of London, B271, 12831291.
Piersma, T. & Everaarts, J.M. 1996. Build-up of red blood cells in refueling bar-tailed godwits in relation to individual migratory quality. Condor, 98, 363370.
Prop, J., Black, J.M. & Shimmings, P. 2003. Travel schedules to the high arctic: barnacle geese trade-off the timing of migration with accumulation of fat deposits. Oikos, 103, 403414.
Rohwer, S., Viggiano, A. & Marzluff, J.M. 2011. Reciprocal tradeoffs between molt and breeding in albatrosses. Condor, 113, 6170.
Romero, L.M. & Fairhurst, G.D. 2016. Measuring corticosterone in feathers: strengths, limitations, and suggestions for the future. Comparative Biochemistry and Physiology - Molecular & Integrative Physiology, 10.1016/j.cbpa.2016.05.002.
Ryan, P.G., Phillips, R.A., Nel, D.C. & Wood, A.G. 2007. Breeding frequency in grey-headed albatrosses Thalassarche chrysostoma . Ibis, 149, 4552.
Silverin, B., Viebke, P.A. & Westin, J. 1989. Hormonal correlates of migration and territorial behavior in juvenile willow tits during autumn. General and Comparative Endocrinology, 75, 148156.
Tickell, W.L.N. 2000. Albatrosses. Sussex: Pica Press, 448 pp.
Vitousek, M.N., Mitchell, M.A., Romero, L.M., Awerman, J. & Wikelski, M. 2010. To breed or not to breed: physiological correlates of reproductive status in a facultatively biennial iguanid. Hormones and Behavior, 57, 140146.
Weimerskirch, H., Delord, K., Guitteaud, A., Phillips, R.A. & Pinet, P. 2015. Extreme variation in migration strategies between and within wandering albatross populations during their sabbatical year, and their fitness consequences. Scientific Reports, 5, 10.1038/srep08853.
Williams, T.D. 2012. Physiological adaptations for breeding in birds. Princeton, NJ: Princeton University Press, 392 pp.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Antarctic Science
  • ISSN: 0954-1020
  • EISSN: 1365-2079
  • URL: /core/journals/antarctic-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed