Abstract
We examined the isotopic signatures (δ13C, δ15N) of adult body feathers from southern giant petrels Macronectes giganteus collected at two breeding colonies in Antarctica (Potter Peninsula and Cape Geddes) and one in southern Patagonia (Observatorio Island), as well as in whole blood collected from adults of both sexes at each Antarctic colonies and from chicks at Potter Peninsula. As body feather moult is a continuous process in giant petrels, feathers provide an integrated annual signal of an adult’s diets and foraging habitats. In contrast, the stable isotope values of adult and chick blood are reflective of their diets during the breeding season. We found that sex-specific dietary segregation in adults breeding in Antarctica was notable during the breeding season (blood samples) but absent when examined across the entire year (feather samples). In addition, blood stable isotope values differed between chicks and adults, indicating that adults provision their offspring with a relatively higher amount of penguin and seal prey that what they consume themselves. This finding confirms previous work that suggests that chicks are preferentially fed with prey of presumably higher nutritional value such as carrion. Finally, based on isotopic differences between major oceanographic zones in the Southern Ocean, our data indicate population-specific differences in foraging distribution, with Antarctic populations move seasonally between Antarctic and subantarctic zones, while Patagonian populations likely forage in subtropical waters and in continental shelf habitats year-round.
Similar content being viewed by others
References
Ainley DG, Ford RG, Brown ED, Suryan RM, Irons DB (2003) Prey resources, competition, and geographic structure of kittiwake colonies in Prince William Sound. Ecology 84:709–723
Anderson ORJ, Phillips RA, McDonald RA, Shore RF, McGill RAR, Bearhop S (2009) Influence of trophic position and foraging range on mercury levels within a seabird community. Mar Ecol Prog Ser 375:277–288
Barrera-Oro E (2002) The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antarct Sci 14:293–309
Bartumeus F, Giuggioli L, Louzao M, Bretagnolle V, Oro D, Levin S (2010) Fishery discards impact on seabird movement patterns at regional scales. Curr Biol 20:215–222
Bearhop S, Teece MA, Waldron S, Furness FW (2000) The influence of uric acid upon δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507
Belkin IM, Gordon AL (1996) Southern ocean fronts from the Greenwich meridian to Tasmania. J Geophys Res 101:3675–3696
Best PB, Schell DM (1996) Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Mar Biol 124:483–494
Boyd IL, Arnbom TA, Fedak MA (1994) Biomass and energy consumption of the South Georgia population of southern elephant seals. In: Le Boeuf BJ, Laws RM (eds) Elephant seals: population ecology, behaviour, and physiology. University of California Press, Berkeley, pp 98–117
Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotopes signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462
Catry P, Phillips RA, Croxall JP (2005) Sexual segregation in birds: patterns, processes and implications for conservation. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation: ecology of the two sexes. Cambridge University Press, Cambridge, pp 351–378
Cherel Y, Hobson KA (2007) Geographical variation in stable carbon 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, Hobson KA, Hassani S (2005) Isotopic discrimination factors between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115
Cherel Y, Phillips RA, Hobson KA, McGill R (2006) Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds. Biol Lett 2:301–303
Cherel Y, Hobson KA, Guinet C, Vanpe C (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
Clarke J, Manly B, Kerry K, Gardner H, Franchi E, Corsolini S, Focardi S (1998) Sex differences in Adélie penguin foraging strategies. Polar Biol 20:248–258
Conroy JWH (1972) Ecological aspects of the biology of the giant petrel Macronectes giganteus (Gmelin) in the maritime Antarctic. Br Antarct Surv Sci Rep 75:1–74
Cook TR, Cherel Y, Bost CA, Tremblay Y (2007) Chick-rearing Crozet shags (Phalacrocorax melanogenis) display sex-specific foraging behaviour. Antarct Sci 19:55–63
Copello S, Quintana F (2009) Spatio-temporal overlap between southern giant petrels and fisheries at the Patagonian shelf. Polar Biol 32:1211–1220
Copello S, Quintana F, Perez F (2008) The diet of the southern giant petrel in Patagonia: fishery-related items and natural prey. Endanger Species Res 6:15–23
Copello S, Dogliotti AI, Gagliardini DA, Quintana F (2011) Oceanographic and biological landscapes used by the southern giant petrel during the breeding season at the Patagonian shelf. Mar Biol 158:1247–1257
Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and Antarctic seabird populations. Science 297:1510–1514
Dahdul WM, Horn MH (2004) Energy allocation and postnatal growth in captive elegant tern (Sterna elegans) chicks: responses to high- versus low-energy diets. Auk 120:1069–1081
Forcada J, Malone D, Royle JA, Staniland IJ (2009) Modelling predation by transient leopard seals for an ecosystem-based management of Southern Ocean fisheries. Ecol Model 220:1513–1521
Forero MG, Hobson KA, Bortolotti GR, Donázar JA, Bertellotti M, Blanco G (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar Ecol Prog Ser 234:289–299
Forero MG, Bortolotti GR, Hobson KA, Donázar JA, Bertellotti M, Blanco G (2004) High trophic overlap within the seabird community of Argentinean Patagonia: a multiscale approach. J Anim Ecol 73:789–801
Forero MG, González-Solís J, Hobson KA, Donázar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113
François R, Altabet MA, Goericke R (1993) Changes in the δ13C of surface water particulate matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem Cycles 7:627–644
Furness RW, Birkhead TR (1984) Seabird colony distributions suggest competition for food supplies during the breeding season. Nature 311:655–656
Gilardi JD (1992) Sex-specific foraging distributions of brown boobies in the eastern tropical Pacific. Colon Waterbirds 15:148–151
Gonzalez Solís J, Shaffer SA (2009) Introduction and synthesis: spatial ecology of seabird at sea. Mar Ecol Prog Ser 391:117–120
González-Solís J, Croxall JP (2005) Differences in foraging behaviour and feeding ecology in giant petrels. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, pp 92–111
González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels Macronectes halli during incubation. Oikos 90:390–398
Gonzalez-Zevallos D, Yorio P (2006) Seabird use of discards and incidental captures at the Argentine hake trawl fishery in the Golfo San Jorge, Argentina. Mar Ecol Prog Ser 316:175–183
Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2009) Using isoscapes to trace the movements and foraging behavior of top predators in Oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern, and process on earth through isotope mapping. Springer, New York, pp 299–318
Grémillet D, Dell’Omo G, Ryan PG, Peters G, Ropert-Coudert Y, Weeks SJ (2004) Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape gannets from neighbouring colonies. Mar Ecol Prog Ser 268:265–279
Habran S, Debier C, Crocker DE, Houser DS, Lepoint G, Bouquegneau JM, Das K (2010) Assessment of gestation, lactation and fasting on stable isotope ratios in northern elephant seals (Mirounga angustirostris). Mar Mammal Sci 26:880–895
Halley DJ, Minagawa M, Nieminen M, Gaare E (2008) Preservation in 70 % ethanol solution does not affect δ13C and δ15N values of reindeer blood samples—relevance for stable isotope studies of diet. Rangifer 28:9–12
Harding AMA, Hobson KA, Wojciech W, Dmoch K, Karnovsky NJ, Van Pelt TI, Lifjeld JT (2008) Can stable isotope (δ13C and δ15N) measurements of little auk (Alle alle) adults and chicks be used to track changes in high-Arctic marine foodwebs? Polar Biol 31:725–733
Hobson KA, Clark RW (1992) Assessing avian diets using stable isotopes. II. Factors influencing diet–tissue fractionation. Condor 94:189–197
Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533
Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable nitrogen isotope analysis. Can J Zool 75:1720–1723
Hodum PJ, Hobson KA (2000) Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable isotope (δ15N and δ13C) analyses. Mar Ecol Prog Ser 198:273–281
Hunter S (1983) The food and feeding of the giant petrels Macronectes halli and M. giganteus at South Georgia. J Zool Lond 200:521–538
Hunter S (1984a) Moult of the giant petrels Macronectes halli and M. giganteus at South Georgia. Ibis 126:119–132
Hunter S (1984b) Breeding biology and population dynamics of giant petrels Macronectes at South Georgia (Aves: Procellariiformes). J Zool Lond 203:441–460
Hunter S, de Brooke M (1992) The diet of giant petrels Macronectes spp. at Marion Island, Southern Indian Ocean. Colon Waterbirds 15:56–65
Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819
Otley H, Reid T, Phillips R, Wood A, Phalan B, Forster I (2007) Origin, age, sex and breeding status of wandering albatrosses (Diomedea exulans), northern (Macronectes halli) and southern giant petrels (Macronectes giganteus) attending demersal longliners in Falkland Islands and Scotia Ridge waters, 2001–2005. Polar Biol 30:359–368
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672
Phillips RA, Bearhop S, Mcgill RAR, Dawson DA (2009) Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period. Oecologia 160:795–806
Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208
Polito MJ, Goebel ME (2010) Investigating the use of stable isotope analysis of milk to infer seasonal trends in the diets and foraging habitats of female Antarctic fur seals. J Exp Mar Biol Ecol 39:1–9
Quillfeldt P, McGill RAR, Furness RW (2005) Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s storm-petrel. Mar Ecol Prog Ser 295:295–304
Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598
Quintana F, Wilson R, Dell’Arciprete P, Shepard E, Gómez Laich A (2011) Women from Venus, men from Mars: inter-sex foraging differences in the Imperial cormorant, Phalacrocorax atriceps, a colonial seabird. Oikos 120:350–358
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/. ISBN 3–900051–07–0
Ramos R, Gonzalez-Solis J, Forero MG et al (2009) The influence of breeding colony and sex on mercury, selenium and lead levels and carbon and nitrogen stable isotope signatures in summer and winter feathers of Calonectris shearwaters. Oecologia 159:345–354
Raya Rey A, Trathan P, Pütz K, Schiavini A (2007) Effect of oceanographic conditions on the winter dispersion of Eudyptes chrysocome chrysocome at Staten Island, Argentina. Mar Ecol Prog Ser 330:285–295
Ricklefs RE, Starck JM, Konarzewski M (1998) Internal constraints on growth in birds. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, Oxford, pp 266–287
Roscales JL, Munoz-Arnanz J, Gonzalez-Solis J, Jimenez B (2010) Geographical PCB and DDT Patterns in Shearwaters (Calonectris sp.) breeding across the NE Atlantic and the Mediterranean Archipelagos. Environ Sci Technol 44:2328–2334
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263
Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabirds stable isotope ratios. Oecologia 159:41–48
Seminoff JA, Bjorndal KA, Bolten AB (2007) Stable carbon and nitrogen isotope discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia (3):534–542
Stegall VK, Farley SD, Rea LD, Pitcher KW, Rye RO, Kester CL, Stricker CA, Bern CR (2008) Discrimination of nitrogen and carbon isotopes from milk to serum and vibrissae in Alaska Steller sea lions (Eumetopias jubatus). Can J Zool 86:17–23
Sullivan BJ, Reid T, Bugoni L (2006) Seabird mortality on factory trawlers in the Falkland Islands and beyond. Biol Conserv 131:495–504
Therrien J-F, Fitzgerald G, Gauthier G, Bêty J (2011) Diet–tissue discrimination factors of carbon and nitrogen stable isotopes in blood of snowy owl (Bubo scandiacus). Can J Zool 89:343–347
Trull TW, Armand L (2001) Insights into Southern Ocean carbon export from the δ13C of particles and dissolved inorganic carbon during the SOIREE iron release experiment. Deep Sea Res II 48:2655–2680
Watanuki Y (1992) Individual diet difference, parental care and reproductive success in slaty-baked gulls. Condor 94:159–171
Weimerskirch H, Shaffer SA, Tremblay Y, Costa DP, Gadenne H, Kato A, Ropert-Coudert Y, Sato K, Aurioles D (2009) Species- and sex specific differences in foraging behaviour and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar Ecol Prog Ser 391:267–278
Williams CT, Buck CL, Sears J, Kitaysky AS (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11–18
Acknowledgments
We would like to thank CONICET and Instituto Antártico Argentino for institutional support. Special thanks to the Argentine Navy for transportation to Staten Island and Dirección Nacional del Antártico for the logistical support to the Antarctic colonies. Thanks to R. Sáenz Samaniego, N. Rosciano, and J. M. Raya Rey for their help in the field. Many thanks to M. Goebel, C. Jones, S. Trivelpiece, W. Trivelpiece, J. Walsh, A. VanCise, and others from the US Antarctic Marine Living Resources (AMLR) program who helped collect the prey samples used in this manuscript. K Durenberger, J Seminoff, and N Spear provided helpful assistance with lipid extractions and stable isotope analysis. Southern giant petrel and penguin samples were collected under approved animal use protocols and Antarctic Conservation Act permits provided by Secretaría de Desarrollo Sustentable y Ambiente and Dirección Nacional del Antártico and the US National Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Garthe.
Rights and permissions
About this article
Cite this article
Raya Rey, A., Polito, M., Archuby, D. et al. Stable isotopes identify age- and sex-specific dietary partitioning and foraging habitat segregation in southern giant petrels breeding in Antarctica and southern Patagonia. Mar Biol 159, 1317–1326 (2012). https://doi.org/10.1007/s00227-012-1912-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-1912-y