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Costs of reproduction and carry-over effects in breeding albatrosses

Part of: Antarctic Science International Bursary collection: Biosciences

Published online by Cambridge University Press:  29 November 2016

Glenn T. Crossin ,
richard A. Phillips ,
Christine R. Lattin ,
L. Michael Romero ,
Xavier Bordeleau ,
Christopher M. Harris ,
Oliver P. Love  and
Tony D. Williams
Glenn T. Crossin*
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
richard A. Phillips
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Christine R. Lattin
Affiliation:
Department of Biology, Tufts University, Medford, MA02155, USA
L. Michael Romero
Affiliation:
Department of Biology, Tufts University, Medford, MA02155, USA
Xavier Bordeleau
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
Christopher M. Harris
Affiliation:
Department of Biological Sciences and Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, Canada
Oliver P. Love
Affiliation:
Department of Biological Sciences and Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, Canada
Tony D. Williams
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada
*
gtc@dal.ca
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Abstract

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.

Keywords

feather corticosteroneglucocorticoidshaematocritmigrationtestosteronetriglycerides
Type
Biological Sciences
Information
Antarctic Science , Volume 29 , Issue 2 , April 2017 , pp. 155 - 164
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Copyright
© Antarctic Science Ltd 2016 

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References

Bonier, F., Martin, P.R., Moore, I.T. & Wingfield, J.C. 2009. Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution, 24, 634–642.Google Scholar
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, 494–500.CrossRefGoogle Scholar
Bugoni, L., Naves, L.C. & Furness, R.W. 2015. Moult of three Tristan da Cunha seabird species sampled at sea. Antarctic Science, 27, 239–251.Google Scholar
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, 837–842.Google Scholar
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, 1–17.Google Scholar
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, 116–125.Google Scholar
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, 761–768.Google Scholar
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, 112–120.CrossRefGoogle ScholarPubMed
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, 151–157.Google Scholar
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, 69–83.Google Scholar
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, 249–250.Google Scholar
Daan, S., Deerenberg, C. & Dijkstra, C. 1996. Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology, 65, 539–544.Google Scholar
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, 671–681.Google Scholar
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, 105–113.CrossRefGoogle Scholar
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, 273–283.Google Scholar
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, 84–98.Google Scholar
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.Google Scholar
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, 4–18.Google Scholar
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, 237–253.Google Scholar
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, 235–243.Google Scholar
Jouventin, P. & Dobson, F.S. 2002. Why breed every other year? The case of albatrosses. Proceedings of the Royal Society of London, B269, 1955–1961.CrossRefGoogle Scholar
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, 501–514.CrossRefGoogle Scholar
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, 413–418.Google Scholar
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, 247–252.Google Scholar
Love, O.P., Breuner, C.W., Vézina, F. & Williams, T.D. 2004. Mediation of a corticosterone-induced reproductive conflict. Hormones and Behavior, 46, 59–65.CrossRefGoogle ScholarPubMed
Monaghan, P. & Nager, R.G. 1997. Why don’t birds lay more eggs? Trends in Ecology & Evolution, 12, 270–272.Google Scholar
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, 189–191.Google Scholar
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, 1731–1735.CrossRefGoogle Scholar
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.Google Scholar
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, 473–477.Google Scholar
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, 121–131.Google Scholar
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, 2386–2396.Google Scholar
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, 1283–1291.Google Scholar
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, 363–370.Google Scholar
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, 403–414.Google Scholar
Rohwer, S., Viggiano, A. & Marzluff, J.M. 2011. Reciprocal tradeoffs between molt and breeding in albatrosses. Condor, 113, 61–70.Google Scholar
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.Google Scholar
Ryan, P.G., Phillips, R.A., Nel, D.C. & Wood, A.G. 2007. Breeding frequency in grey-headed albatrosses Thalassarche chrysostoma . Ibis, 149, 45–52.Google Scholar
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, 148–156.Google Scholar
Tickell, W.L.N. 2000. Albatrosses. Sussex: Pica Press, 448 pp.Google Scholar
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, 140–146.Google Scholar
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.CrossRefGoogle ScholarPubMed
Williams, T.D. 2012. Physiological adaptations for breeding in birds. Princeton, NJ: Princeton University Press, 392 pp.Google Scholar