seabirds; stable isotopes; Sub Antarctic; global climate change
Abstract :
[en] Individual specialization in diet or foraging behavior within apparently generalist
populations has been described for many species, especially in polar and
temperate marine environments, where resource distribution is relatively predictable.
It is unclear, however, whether and how increased environmental variability
– and thus reduced predictability of resources – due to global climate
change will affect individual specialization. We determined the within- and
among-individual components of the trophic niche and the within-individual
repeatability of d13C and d15N in feathers and red blood cells of individual
female southern rockhopper penguins (Eudyptes chrysocome) across 7 years. We
also investigated the effect of environmental variables (Southern Annular Mode,
Southern Oscillation Index, and local sea surface temperature anomaly) on the
isotopic values, as well as the link between stable isotopes and female body
mass, clutch initiation dates, and total clutch mass. We observed consistent red
blood cell d13C and d15N values within individuals among years, suggesting a
moderate degree of within-individual specialization in C and N during the prebreeding
period. However, the total niche width was reduced and individual
specialization not present during the premolt period. Despite significant interannual
differences in isotope values of C and N and environmental conditions,
none of the environmental variables were linked to stable isotope values and
thus able to explain phenotypic plasticity. Furthermore, neither the within-individual
nor among-individual effects of stable isotopes were found to be related
to female body mass, clutch initiation date, or total clutch mass. In conclusion,
our results emphasize that the degree of specialization within generalist populations
can vary over the course of 1 year, even when being consistent within the
same season across years. We were unable to confirm that environmental variability
counteracts individual specialization in foraging behavior, as phenotypic
plasticity in d13C and d15N was not linked to any of the environmental variables
studied.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Dehnhard, Nina; Universiteit Antwerpen - UA > Dept. Biology > Behavioural Ecology & Ecophysiology Group
Eens, Marcel; Universiteit Antwerpen - UA > Dept. Biology > Behavioural Ecology & Ecophysiology Group
Sturaro, Nicolas ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Lepoint, Gilles ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Demongin, Laurent; Universiteit Antwerpen - UA > Dept. Biology > Behavioural Ecology & Ecophysiology Group
Quillfeldt, Petra; Universiteit Antwerpen - UA > Dept. Biology > Behavioural Ecology & Ecophysiology Group
Poisbleau, Maud; Universiteit Antwerpen - UA > Dept. Biology > Behavioural Ecology & Ecophysiology Group
Language :
English
Title :
Is individual consistency in body mass and reproductive decisions linked to individual specialization in foraging behavior in a long-lived seabird?
Publication date :
2016
Journal title :
Ecology and Evolution
eISSN :
2045-7758
Publisher :
Wiley
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen DFG - Deutsche Forschungsgemeinschaft Environmental Studies Budget grant from the Falkland Islands Governmen
Anderson, O. R. J., R. A. Phillips, R. F. Shore, R. A. R. McGill, R. A. McDonald, and S. Bearhop. 2009. Diet, individual specialisation and breeding of brown skuas (Catharacta antarctica lonnbergi): an investigation using stable isotopes. Polar Biol. 32:27–33.
Annett, C. A., and R. Pierotti. 1999. Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297.
Araújo, M. S., D. I. Bolnick, and C. A. Layman. 2011. The ecological causes of individual specialisation. Ecol. Lett. 14:948–958.
Bates, D., M. Maechler, and B. Bolker. 2011. lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. Available at http://CRAN.R-project.org/package=lme4.
Baylis, A. M., A. F. Zuur, P. Brickle, and P. A. Pistorius. 2012. Climate as a driver of population variability in breeding gentoo penguins Pygoscelis papua at the Falkland Islands. The Ibis 154:30–41.
Baylis, A. M. M., R. A. Orben, J. P. Y. Arnould, K. Peters, T. Knox, D. P. Costa, et al. 2015. Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia 179:1053–1065.
Bearhop, S., S. Waldron, S. C. Votier, and R. W. Furness. 2002. Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol. Biochem. Zool. 75:451–458.
Bearhop, S., C. E. Adams, S. Waldron, R. A. Fuller, and H. MacLeod. 2004. Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol. 73:1007–1012.
Behrenfeld, M. J., R. T. O'Malley, D. A. Siegel, C. R. McClain, J. L. Sarmiento, G. C. Feldman, et al. 2006. Climate-driven trends in contemporary ocean productivity. Nature 444:752–755.
Bolnick, D. I., R. Svanbäck, J. A. Fordyce, L. H. Yang, J. M. Davis, C. D. Hulsey, et al. 2003. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161:1–28.
Ceia, F., R. Phillips, J. Ramos, Y. Cherel, R. Vieira, P. Richard, et al. 2012. Short- and long-term consistency in the foraging niche of wandering albatrosses. Mar. Biol. 159:1581–1591.
Cherel, Y., and K. A. Hobson. 2007. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar. Ecol. Prog. Ser. 329:281–287.
Cherel, Y., K. A. Hobson, F. Bailleul, and R. Groscolas. 2005a. Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888.
Cherel, Y., K. A. Hobson, and S. Hassani. 2005b. Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol. Biochem. Zool. 78:106–115.
Cherel, Y., K. A. Hobson, C. Guinet, and C. Vanpe. 2007. Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J. Anim. Ecol. 76:826–836.
Cimino, M., W. Fraser, D. Patterson-Fraser, V. Saba, and M. Oliver. 2014. Large-scale climate and local weather drive interannual variability in Adélie penguin chick fledging mass. Mar. Ecol. Prog. Ser. 513:253–268.
Dehnhard, N., C. C. Voigt, M. Poisbleau, L. Demongin, and P. Quillfeldt. 2011. Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period. Polar Biol. 34:1763–1773.
Dehnhard, N., K. Ludynia, M. Poisbleau, L. Demongin, and P. Quillfeldt. 2013a. Good days, bad days: wind as a driver of foraging success in a flightless seabird, the southern rockhopper penguin. PLoS ONE 8:e79487.
Dehnhard, N., M. Poisbleau, L. Demongin, K. Ludynia, M. Lecoq, J. F. Masello, et al. 2013b. Survival of rockhopper penguins in times of global climate change. Aquat. Conserv. 23:777–789.
Dehnhard, N., M. Eens, L. Demongin, P. Quillfeldt, and M. Poisbleau. 2015a. Individual consistency and phenotypic plasticity in rockhopper penguins: female but not male body mass links environmental conditions to reproductive investment. PLoS ONE 10:e0128776.
Dehnhard, N., M. Eens, L. Demongin, P. Quillfeldt, D. Suri, and M. Poisbleau. 2015b. Limited individual phenotypic plasticity in the timing of and investment into egg laying in southern rockhopper penguins under climate change. Mar. Ecol. Prog. Ser. 524:269–281.
Dingemanse, N. J., and M. Wolf. 2013. Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim. Behav. 85:1031–1039.
Ducatez, S., S. Dalloyau, P. Richard, C. Guinet, and Y. Cherel. 2008. Stable isotopes document winter trophic ecology and maternal investment of adult female southern elephant seals (Mirounga leonina) breeding at the Kerguelen Islands. Mar. Biol. 155:413–420.
Durant, J. M., D. O. Hjermann, G. Ottersen, and N. C. Stenseth. 2007. Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33:271–283.
Durant, J., R. Crawford, A. Wolfaardt, K. Agenbag, J. Visagie, L. Upfold, et al. 2010. Influence of feeding conditions on breeding of African penguins – importance of adequate local food supplies. Mar. Ecol. Prog. Ser. 420:263–271.
Emmerson, L., R. Pike, and C. Southwell. 2011. Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology. Mar. Ecol. Prog. Ser. 440:203–216.
Frederiksen, M., M. P. Harris, F. Daunt, P. Rothery, and S. Wanless. 2004. Scale-dependent climate signals drive breeding phenology of three seabird species. Glob. Change Biol. 10:1214–1221.
Frederiksen, M., M. Edwards, R. A. Mavor, and S. Wanless. 2007. Regional and annual variation in black-legged kittiwake breeding productivity is related to sea surface temperature. Mar. Ecol. Prog. Ser. 350:137–143.
Gienapp, P., C. Teplitsky, J. S. Alho, J. A. Mills, and J. Merilä. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17:167–178.
Green, J. A., I. L. Boyd, A. J. Woakes, N. L. Warren, and P. J. Butler. 2009. Evaluating the prudence of parents: daily energy expenditure throughout the annual cycle of a free-ranging bird, the Macaroni penguin Eudyptes chrysolophus. J. Avian Biol. 40:529–538.
Hammerschlag, N., D. Ovando, and J. E. Serafy. 2010. Seasonal diet and feeding habits of juvenile fishes foraging along a subtropical marine ecotone. Aquat. Biol. 9:279–290.
Herrera, M. L. G., C. Korine, T. H. Fleming, and Z. Arad. 2008. Dietary implications of intrapopulation variation in nitrogen isotope composition of an old world fruit bat. J. Mammal. 89:1184–1190.
Hindell, M. A., C. J. Bradshaw, B. W. Brook, D. A. Fordham, K. Kerry, C. Hull, et al. 2012. Long-term breeding phenology shift in royal penguins. Ecol. Evol. 2:1563–1571.
Hinke, J. T., M. J. Polito, M. E. Goebel, S. Jarvis, C. S. Reiss, S. R. Thorrold, et al. 2015. Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands. Ecosphere 6:125.
Hobson, K. A., R. T. Alisauskas, and R. G. Clark. 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394.
Houston, A., and J. M. McNamara. 1992. Phenotypic plasticity as a state-dependent life-history decision. Evol. Ecol. 6:243–253.
Jaeger, A., P. Blanchard, P. Richard, and Y. Cherel. 2009. Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar. Biol. 156:1233–1240.
Jaeger, A., M. Connan, P. Richard, and Y. Cherel. 2010. Use of stable isotopes to quantify seasonal changes of trophic niche and levels of population and individual specialisation in seabirds. Mar. Ecol. Prog. Ser. 401:269–277.
Keymer, I. F., H. M. Malcolm, A. Hunt, and D. T. Horsley. 2001. Health evaluation of penguins (Sphenisciformes) following mortality in the Falklands (South Atlantic). Dis. Aquat. Organ. 45:159–169.
Kim, S. L., and P. L. Koch. 2012. Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ. Biol. Fishes 95:53–63.
Kowalczyk, N. D., A. Chiaradia, T. J. Preston, and R. D. Reina. 2014. Linking dietary shifts and reproductive failure in seabirds: a stable isotope approach. Funct. Ecol. 28:755–765.
Kwok, R., and J. C. Comiso. 2002. Southern ocean climate and sea ice anomalies associated with the Southern Oscillation. J. Clim. 15:487–501.
Lemons, G. E., T. Eguchi, B. N. Lyon, R. LeRoux, and J. A. Seminoff. 2012. Effects of blood anticoagulants on stable isotope values of sea turtle blood tissue. Aquat. Biol. 14:201–206.
Ludynia, K., N. Dehnhard, M. Poisbleau, L. Demongin, J. F. Masello, and P. Quillfeldt. 2012. Evaluating the impact of handling and logger attachment on foraging parameters and physiology in southern rockhopper penguins. PLoS ONE 7:e50429.
Ludynia, K., N. Dehnhard, M. Poisbleau, L. Demongin, J. F. Masello, C. C. Voigt, et al. 2013. Sexual segregation in rockhopper penguins during incubation. Anim. Behav. 85:255–267.
Lynch, H. J., W. F. Fagan, R. Naveen, S. G. Trivelpiece, and W. Z. Trivelpiece. 2012. Differential advancement of breeding phenology in response to climate may alter staggered breeding among sympatric pygoscelid penguins. Mar. Ecol. Prog. Ser. 454:135–145.
Mann, K. H., and J. R. N. Lazier. 2006. Dynamics of marine ecosystems: biological-physical interactions in the oceans, 3rd ed. Blackwell Publishing Ltd, Oxford, UK.
Marshall, G. J. 2003. Trends in the Southern Annular Mode from observations and reanalyses. J. Clim. 16:4134–4143.
Masello, J. F., M. Wikelski, C. C. Voigt, and P. Quillfeldt. 2013. Distribution patterns predict individual specialization in the diet of dolphin gulls. PLoS ONE 8:e67714.
Meredith, M. P., E. J. Murphy, E. J. Hawker, E. J. Hawker, J. C. King, and M. I. Wallace. 2008. On the interannual variability of ocean temperatures around South Georgia, Southern Ocean: forcing by El Niño/Southern Oscillation and the Southern Annular Mode. Deep-Sea Res. II 55:2007–2022.
Minagawa, M., and E. Wada. 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta 48:1135–1140.
Moline, M. A., H. Claustre, T. K. Frazer, O. Schofield, and M. Vernet. 2004. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob. Change Biol. 10:1973–1980.
Nakagawa, S., and H. Schielzeth. 2010. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85:935–956.
Nakagawa, S., and H. Schielzeth. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4:133–142.
Nussey, D. H., T. H. Clutton-Brock, D. A. Elston, S. D. Albon, and L. E. B. Kruuk. 2005a. Phenotypic plasticity in a maternal trait in red deer. J. Anim. Ecol. 74:387–396.
Nussey, D. H., E. Postma, P. Gienapp, and M. E. Visser. 2005b. Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306.
Nussey, D. H., A. J. Wilson, and J. E. Brommer. 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20:831–844.
Parrish, J. D. 1997. Patterns of frugivory and energetic condition in Nearctic landbirds during autumn migration. Condor 99:681–697.
Patrick, S. C., and H. Weimerskirch. 2014. Personality, foraging and fitness consequences in a long lived seabird. PLoS ONE 9:e87269.
Poisbleau, M., L. Demongin, H. J. van Noordwijk, I. J. Strange, and P. Quillfeldt. 2010. Sexual dimorphism and use of morphological measurements to sex adults, immatures and chicks of rockhopper penguins. Ardea 98:217–227.
Polito, M. J., W. Z. Trivelpiece, W. P. Patterson, N. J. Karnovsky, C. S. Reiss, and S. D. Emslie. 2015. Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Mar. Ecol. Prog. Ser. 519:221–237.
Pütz, K., A. R. Rey, A. Schiavini, A. P. Clausen, and B. H. Lüthi. 2006. Winter migration of rockhopper penguins (Eudyptes c. chrysocome) breeding in the Southwest Atlantic: is utilisation of different foraging areas reflected in opposing population trends? Polar Biol. 29:735–744.
Pütz, K., A. Raya Rey, and H. Otley. 2013. Southern rockhopper penguin. Pp. 113–129 in P. G. Borboroglu and P. D. Boersma, eds. Penguins – natural history and conservation. University of Washington Press, Seattle, WA.
Quillfeldt, P., J. F. Masello, R. A. R. McGill, M. Adams, and R. W. Furness. 2010. Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Front. Zool. 7:15.
Quillfeldt, P., K. Ekschmitt, P. Brickle, R. A. R. McGill, V. Wolters, N. Dehnhard, et al. 2015. Variability of higher trophic level stable isotope data in space and time – a case study in a marine ecosystem. Rapid Commun. Mass Spectrom. 29:667–674.
R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.
Ratcliffe, N., S. Crofts, R. Brown, A. M. M. Baylis, S. Adlard, C. Horswill, et al. 2014. Love thy neighbour or opposites attract? Patterns of spatial segregation and association among crested penguin populations during winter. J. Biogeogr. 41:1183–1192.
Roughgarden, J. 1972. Evolution of niche width. Am. Nat. 106:683–718.
Rubenstein, D. R., and K. A. Hobson. 2004. From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol. Evol. 19:256–263.
Schielzeth, H., and S. Nakagawa. 2013. rptR: repeatability for Gaussian and non-Gaussian data. R package version 0.6.405/r52. Available at http://R-Forge.R-project.org/projects/rptr.
Schoener, T. W. 1971. Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2:369–404.
Spear, L. B. 1993. Dynamics and effect of western gulls feeding in a colony of guillemots and Brandt's cormorants. J. Anim. Ecol. 62:399–414.
Stamps, J., and T. G. G. Groothuis. 2010. The development of animal personality: relevance, concepts and perspectives. Biol. Rev. 85:301–325.
Strange, I. J. 1982. Breeding ecology of the rockhopper penguin (Eudyptes crestatus) in the Falkland Islands. Gerfaut 72:137–188.
Thiebot, J. B., Y. Cherel, M. Acqueberge, A. Prudor, P. N. Trathan, and C. A. Bost. 2014. Adjustment of pre-moult foraging strategies in macaroni penguins Eudyptes chrysolophus according to locality, sex and breeding status. The Ibis 156:511–522.
Thiebot, J.-B., C.-A. Bost, N. Dehnhard, L. Demongin, M. Eens, G. Lepoint, et al. 2015. Mates but not sexes differ in migratory niche in a monogamous penguin species. Biol. Lett. 11:20150429.
van de Pol, M., and J. Wright. 2009. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77:753–758.
van de Pol, M., L. Brouwer, B. J. Ens, K. Oosterbeek, and J. M. Tinbergen. 2010. Fluctuating selection and the maintenance of individual and sex-specific diet specialization in free-living oystercatchers. Evolution 64:836–851.
van Gils, J. A., P. F. Battley, T. Piersma, and R. Drent. 2005. Reinterpretation of gizzard sizes of red knots world-wide emphasises overriding importance of prey quality at migratory stopover sites. Proc. Biol. Sci. 272:2609–2618.
Vedder, O., S. Bouwhuis, and B. C. Sheldon. 2013. Quantitative assessment of the importance of phenotypic plasticity in adaptation to climate change in wild bird populations. PLoS Biol. 11:e1001605.
Veit, R. R., and L. L. Manne. 2015. Climate and changing winter distribution of alcids in the Northwest Atlantic. Front. Ecol. Evol. 3:38.
Votier, S. C., S. Bearhop, N. Ratcliffe, and R. W. Furness. 2004. Reproductive consequences for great skuas specializing as seabird predators. Condor 106:275–287.
Votier, S. C., S. Bearhop, M. J. Witt, R. Inger, D. Thompson, and J. Newton. 2010. Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J. Appl. Ecol. 47:487–497.
Wakefield, E. D., I. R. Cleasby, S. Bearhop, T. W. Bodey, R. D. Davies, P. I. Miller, et al. 2015. Long-term individual foraging site fidelity—why some gannets don't change their spots. Ecology 96:3058–3074.
Warham, J. 1963. The rockhopper penguin, Eudoptes chrysocome, at Macquarie Island. Auk 80:229–256.
Watanuki, Y., A. Takahashi, and K. Sato. 2010. Individual variation of foraging behavior and food provisioning in Adélie penguins (Pygoscelis adeliae) in a fast-sea-ice area. Auk 127:523–531.
Weimerskirch, H. 2007. Are seabirds foraging for unpredictable resources? Deep-Sea Res. II 54:211–223.
Weiss, F., R. W. Furness, R. A. R. McGill, I. J. Strange, J. F. Masello, and P. Quillfeldt. 2009. Trophic segregation of Falkland Islands seabirds: insights from stable isotope analysis. Polar Biol. 32:1753–1763.
Woo, K. J., K. H. Elliot, M. Davidson, A. J. Gaston, and D. K. Davoren. 2008. Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J. Anim. Ecol. 77:1082–1091.
Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extension in ecology with R. Springer, New York, NY.