Diferencias estacionales en la dieta de individuos juveniles del Pingüino Patagónico (Spheniscus magellanicus) reveladas en base al análisis de isótopos estables en uñas

Laura A. Silva; Laura Siles; Luis Cardona; Mauricio Tavares; Enrique Crespo; Patricia Gandini

doi:10.56178/eh.v30i2.582

Articles Published 01 December 2015 https://doi.org/10.56178/eh.v30i2.582

Seasonal diet of Magellanic Penguin (Spheniscus magellanicus) juveniles revealed with a stable isotopes analysis of claws

claws isotopes juveniles SIAR SIBER Spheniscus magellanicus winter diet

Laura A. Silva Laboratorio de Mamíferos Marinos, Centro Nacional Patagónico (CONICET). Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina

Laura Siles IRBIO y Departamento de Biología Evolutiva, Ecología y Ciencias Ambientales, Facultad de Biología, Universidad de Barcelona. Av. Diagonal 643, 08028 Barcelona, España

Luis Cardona IRBIO y Departamento de Biología Evolutiva, Ecología y Ciencias Ambientales, Facultad de Biología, Universidad de Barcelona. Av. Diagonal 643, 08028 Barcelona, España

Mauricio Tavares Centro de Estudos Costeiros, Limnológicos e Marinhos, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (CECLIMAR/IB/UFRGS) y Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS). Av. Tramandaí 976, 95625000 Imbé, Brasil

Enrique Crespo Laboratorio de Mamíferos Marinos, Centro Nacional Patagónico (CONICET). Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina

Patricia Gandini Centro de Investigaciones de Puerto Deseado, Universidad Nacional de la Patagonia Austral. Av. Prefectura Naval s/n, 9050 Puerto Deseado, Santa Cruz, Argentina

Abstract

We carried out a stable isotopes analysis on claws to evaluate the diet and the use of trophic resources of Magellanic Penguin (Spheniscus magellanicus) juveniles off Brazil coasts. The analysis was performed on the basal and distal portions of the claws which correspond to wintering and reproductive seasons, respectively, according to the integration time of the isotopic signature based on the growth rate of claws and sample collection date. We found differences in the isotopic signals between winter and reproductive diets, suggesting differences in the relative contribution of different prey. During the wintering season in Brazil there was a high contribution of Loligo sanpaulensis and anchoita, whereas during the breeding season there was a more diverse contribution of prey items, with an important presence of fishes. Consequently, the isotopic niche breadth was higher in reproductive birds which indicates a broader use of trophic resources in breeding areas. We report a higher consumption of anchoita for juvenile individuals in wintering areas compared to previous studies.

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References

BARQUETE V, STRAUSS V Y RYAN PG (2013) Stable iso-tope turnover in blood and claws: a case study incaptive African penguins. Journal of ExperimentalMarine Biology and Ecology 448:121–127
BEARHOP S, ADAMS CE, WALDRON S, FULLER RA YMACLEOD H (2004) Determining trophic nichewidth: a novel approach using stable isotope analy-sis. Journal of Animal Ecology 73:1007–1012
BEARHOP S, FURNESS RW, HILTON G Y VOTIER SC (2003)A forensic approach to understanding diet andhabitat use from stable isotope analysis of (avian)claw material. Functional Ecology 17:270–275
BERTELLOTTI M, TELLA JL, GODOY JA, BLANCO G,FORERO MG, DONÁZAR JA Y CEBALLOS O (2002)Determining sex of Magellanic Penguins using mo-lecular procedures and discriminant functions.Waterbirds 25:479–484
BOERSMA PD, RESBSTOCK GA, FRERE E Y MOOREL SE(2009) Following the fish: penguins and productiv-ity in the South Atlantic. Ecological Monographs79:59–76
CHEREL Y, HOBSON KA, GUINET C Y VANPE C (2007)Stable isotope document seasonal changes introphic niches and winter foraging individual spe-cialization in diving predators from the SouthernOcean. Journal of Animal Ecology 76:826–836
CHEREL Y, HOBSON KA Y WEIMERSKIRCH H (2000) Usingstable-isotope analysis of feathers to distinguishmoulting and breeding origins of seabirds. Oecologia122:155–162
CHEREL Y, PHILLIPS RA, HOBSON KA Y MC GILL R (2006)Stable isotope evidence of diverse species-specificand individual wintering strategies in seabirds.Biology Letters 2:301–303
CROXALL JP Y PRINCE PA (1996) Cephalopods as prey.I. Seabirds. Philosophical Transactions of the Royal So-ciety of London B 351:1023–1043
DI BENEDITTO AP, AGUIARDOS SANTOS R, RUSSEL R YSALVATORE S (2015) Magellanic penguins: stomachcontents and isotopic profiles to assess the feedingdemands of juveniles in a wintering area off Brazil.Journal of the Marine Biological Association of the UnitedKingdom 95:423–430
DRAGO M, CRESPO E, AGUILAR A, CARDONA L, GARCÍAN, DANS SL Y GOODALL N (2009) Historic diet changeof the South American sea lion in Patagonia asrevealed by isotopic analysis. Marine Ecology ProgressSeries 384:273–286
ETHIER DM, KYLE CJ, KYSER TK Y NOCERA JJ (2010)Variability in the growth patterns of the cornifiedclaw sheath among vertebrates: implications forusing biogeochemistry to study animal movement.Canadian Journal of Zoology 88:1043–1051
FONSECA VS, PETRY MV Y JOST AH (2010) Diet of theMagellanic Penguin on the coast of Rio Grande doSul, Brazil. Waterbirds 24:290–293
FORERO MG, HOBSON KA, BORTOLOTTI GR, DONÁZARJA, BERTELLOTTI M Y BLANCO G (2002) Food resourceutilisation by the Magellanic penguin evaluatedthrough stable-isotope analysis: segregation by sexand age and influence on offspring quality. MarineEcology Progress Series 234:289–299
FRERE E, GANDINI P Y LICHTSCHEIN V (1996) Variaciónlatitudinal en la dieta del pingüino de Magallanes(Spheniscus magellanicus) en la costa patagónica,Argentina. Ornitología Neotropical 7:35–41
FURNESS BL, LAUGKSCH RC Y DUFFY DC (1984)Cephalopods beaks and studies of seabirds diets.Auk 101:619–620
GARCÍA-BORBOROGLU P, BOERSMA PD, RUOPPOLO V,PINHO-DA-SILVA-FILHO R, CORRADO-ADORNES A,CONTE-SENA D, VELOZO R, MYIAJI-KOLESNIKOVAS C,DUTRA G, MARACINI P, CARVALHO-DO-NASCIMENTO C,RAMOS-JÚNIOR V, BARBOSA L Y SERRA S (2010)Magellanic penguin mortality in 2008 along theSW Atlantic coast. Marine Pollution Bulletin60:1652–1657
GONZÁLEZ-SOLÍS J, SMYRLI M, MILITÃO T, GREMILLET D,TYERAA T, PHILLIPS R Y BOULINIER T (2011) Combin-ing stable isotope analyses and geolocation to revealkittiwake migration. Marine Ecology Progress Series435:251–261
HOBSON KA (1999) Tracing origins and migration ofwildlife using stable isotopes: a review. Oecologia120:314–326
HOBSON KA, ALISAUSKAS RT Y CLARK RG (1993) Sta-ble-nitrogen isotope enrichment in avian tissuesdue to fasting and nutritional stress: implicationsfor isotopic analyses of diet. Condor 95:388–394
HOBSON KA Y CLARK RG (1992a) Assessing avian dietsusing stable isotopes I: turnover of 13C in tissues.Condor 94:181–188
HOBSON KA Y CLARK RG (1992b) Assessing avian dietsusing stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197
HOBSON KA, PIATT JF Y PITOCCHELLI J (1994) Using sta-ble isotopes to determine seabird trophic relation-ships. Journal of Animal Ecology 63:786–798INGER R Y BEARHOP S (2008) Applications of stable iso-tope analyses to avian ecology. Ibis 150:447–461
JACKSON AL, INGER R, PARNELL AC Y BEARHOP S (2011)Comparing isotopic niche widths among andwithin communities: SIBER — Stable IsotopeBayesian Ellipses in R. Journal of Animal Ecology80:595–602
JAEGER A, CONNAN P, RICHARD P Y CHEREL Y (2010) Useof stable isotopes to quantify seasonal changes oftrophic niche and levels of population and indi-vidual specialisation in seabirds. Marine EcologyProgress Series 401:269–277
JOBLING M Y BREIBY A (1986) The use and abuse offish otoliths in studies of feeding habits of marinepiscivores. Sarsia 71:265–274
KELLY JF (2000) Stable isotopes of carbon and nitro-gen in the study of avian and mammalian trophicecology. Canadian Journal of Zoology 78:1–27
MÄDER A, SANDER M Y CASA G (2010) Ciclo sazonal demortalidade do influenciado por fatores antrópicose climáticos na costa do Rio Grande do Sul, Brasil.Revista Brasileira de Ornitologia 18:228–233
MARTINEZDEL RÍO C, WOLF S, CARLETON SA Y GANNESLZ (2009) Isotopic ecology ten years after a call formore laboratory experiments. Biological Reviews ofthe Cambridge Philosophical Society 84:91–111
MIZUTANI H, FUKUDA M Y KABAYA Y (1992) 13C and 15Nenrichment factors of feathers of 11 species of adultbirds. Ecology 73:1391–1395
MIZUTANI H, FUKUDA M, KABAYA Y Y WADA E (1990)Carbon isotope ratio of feathers reveals feedingbehavior of cormorants. Auk 107:400–403
NEVES VC, BOLTON M Y MONTEIRO LR (2006) Valida-tion of the water offloading technique for diet as-sessment: an experimental study with Cory ’sshearwaters (Calonectris diomedea). Journal of Orni-thology 147:474–478
PEARSON SF, LAVEY DJ, GREENBERG CH Y MARTÍNEZDELRÍO C (2003) Effects of elemental composition onthe incorporation of dietary nitrogen and carbonisotopic signatures in an omnivorous songbird.Oecologia 135:516–523
PINTO MBLC, SICILIANO S Y DI BENEDITTO APM (2007)Stomach contents of the Magellanic penguinSpheniscus magellanicus from the northern distribu-tion limit on the Atlantic coast of Brazil. MarineOrnithology 35:77–78
PÜTZ K, INGHAM RJ Y SMITH JG (2000) Satellite track-ing of the winter migration of Magellanic PenguinsSpheniscus magellanicus breeding in the FalklandIslands. Ibis 142:614–622
PÜTZ K, SCHIAVINI A, RAYA-REY A Y LUTHI B (2007) Win-ter migration of Magellanic penguins (Spheniscusmagellanicus) from the southernmost distributionalrange. Marine Biology 152:1227–1235
QUILLFELDT P, MCGILL RAR Y FURNESS RW (2005) Dietand foraging areas of Southern Ocean seabirds andtheir prey inferred from stable isotopes: review andcase study of Wilson’s storm-petrel. Marine EcologyProgress Series 295:295–304
RANDALL RM, RANDALL BM Y KLINGELHOEFFER EW(1981) Species diversity and size ranges of cephalo-pods in the diet of Jackass penguins from Algoa Bay,South Africa. South African Journal of Zoology16:163–166
RAYA-REY A, PÜTZ K, SCIOSCIA G, LÜTHI B Y SCHIAVINIA (2012) Sexual differences in the foraging behav-iour of Magellanic Penguins related to stage ofbreeding. Emu 112:90–96
RYAN PG, WILSON RP Y COOPER J (1987) Intraspecificmimicry and status signals in juvenile African pen-guins. Behavioral Ecology and Sociobiology 20:69–76
SCHEINER SM Y GUREVITCH J (2001) Design and analysisof ecological experiments. Segunda edición. OxfordUniversity Press, Oxford
SCHIAVINI A, YORIO P, GANDINI P, RAYA-REY A Y BOERSMAPD (2005) Los pingüinos de las costas argentinas:estado poblacional y conservación. Hornero 20:5–23
SCOLARO JA (1984) Revisión sobre la biología de lareproducción del pingüino de Magallanes. El ciclobiológico anual. Contribuciones Científicas del CentroNacional Patagónico 91:1–26
SCOLARO JA, WILSON R, LAURENTI S, KIERSPEL M,GALLELI H Y UPTON J (1999) Feeding preferences ofthe Magellanic penguin over its breeding range inArgentina. Waterbirds 22:104–110
SILVA L, SAPORITI F, VALES D, TAVARES M, GANDINI P,CRESPO EA Y CARDONA L (2014) Differences in dietcomposition and foraging patterns between sexesof the Magellanic penguin (Spheniscus magellanicus)during the non-breeding period as revealed by δ13Cand δ15N values in feathers and bone. Marine Biol-ogy 161:1195–1206
THOMPSON DR, FURNESS RW Y LEWIS SA (1995) Dietsand long-term changes in δ15N and δ13C values innorthern fulmars Fulmarus glacialis from two north-east Atlantic colonies. Marine Ecology Progress Series125:3–11
TIESZEN LL, BOUTTON TW, TESDAHL KG Y SLADE NA(1983) Fractionation and turnover of stable carbonisotopes in animal tissues: implications for δ13Canalysis of diet. Oecologia 57:32–37
WILSON RP, LA COCK GD, WILSON MP Y MOLLAGEE F(1985) Differential digestion of fish and squid inJackass Penguins Spheniscus demersus. Ornis Scandi-navica 16:77–79
WILSON RP, MANDY A, KIERSPEL M, SCOLARO A,LAURENTI S, UPTON J, GALLELLI H, FRERE E Y GANDINIP (1999) To think or swim: does it really cost pen-guins more to waddle? Journal of Avian Biology30:221–224
WILSON RP, SCOLARO JA, GRÉMILLET D, KIERSPEL MAM,LAURENTI S, UPTON J, GALLELLI H, QUINTANA F, FREREE Y MÜLLER G (2005) How do Magellanic Penguinscope with variability in their access to prey? Eco-logical Monographs 75:379–401

How to cite

Laura A. Silva, Laura Siles, Luis Cardona, Mauricio Tavares, Enrique Crespo, Patricia Gandini (2015). Seasonal diet of Magellanic Penguin (Spheniscus magellanicus) juveniles revealed with a stable isotopes analysis of claws. El Hornero, Vol. 30 No. 2 (2015), 45-54. https://doi.org/10.56178/eh.v30i2.582

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[1] BARQUETE V, STRAUSS V Y RYAN PG (2013) Stable iso-tope turnover in blood and claws: a case study incaptive African penguins. Journal of ExperimentalMarine Biology and Ecology 448:121–127

[2] BEARHOP S, ADAMS CE, WALDRON S, FULLER RA YMACLEOD H (2004) Determining trophic nichewidth: a novel approach using stable isotope analy-sis. Journal of Animal Ecology 73:1007–1012

[3] BEARHOP S, FURNESS RW, HILTON G Y VOTIER SC (2003)A forensic approach to understanding diet andhabitat use from stable isotope analysis of (avian)claw material. Functional Ecology 17:270–275

[4] BERTELLOTTI M, TELLA JL, GODOY JA, BLANCO G,FORERO MG, DONÁZAR JA Y CEBALLOS O (2002)Determining sex of Magellanic Penguins using mo-lecular procedures and discriminant functions.Waterbirds 25:479–484

[5] BOERSMA PD, RESBSTOCK GA, FRERE E Y MOOREL SE(2009) Following the fish: penguins and productiv-ity in the South Atlantic. Ecological Monographs79:59–76

[6] CHEREL Y, HOBSON KA, GUINET C Y VANPE C (2007)Stable isotope document seasonal changes introphic niches and winter foraging individual spe-cialization in diving predators from the SouthernOcean. Journal of Animal Ecology 76:826–836

[7] CHEREL Y, HOBSON KA Y WEIMERSKIRCH H (2000) Usingstable-isotope analysis of feathers to distinguishmoulting and breeding origins of seabirds. Oecologia122:155–162

[8] CHEREL Y, PHILLIPS RA, HOBSON KA Y MC GILL R (2006)Stable isotope evidence of diverse species-specificand individual wintering strategies in seabirds.Biology Letters 2:301–303

[9] CROXALL JP Y PRINCE PA (1996) Cephalopods as prey.I. Seabirds. Philosophical Transactions of the Royal So-ciety of London B 351:1023–1043

[10] DI BENEDITTO AP, AGUIARDOS SANTOS R, RUSSEL R YSALVATORE S (2015) Magellanic penguins: stomachcontents and isotopic profiles to assess the feedingdemands of juveniles in a wintering area off Brazil.Journal of the Marine Biological Association of the UnitedKingdom 95:423–430

[11] DRAGO M, CRESPO E, AGUILAR A, CARDONA L, GARCÍAN, DANS SL Y GOODALL N (2009) Historic diet changeof the South American sea lion in Patagonia asrevealed by isotopic analysis. Marine Ecology ProgressSeries 384:273–286

[12] ETHIER DM, KYLE CJ, KYSER TK Y NOCERA JJ (2010)Variability in the growth patterns of the cornifiedclaw sheath among vertebrates: implications forusing biogeochemistry to study animal movement.Canadian Journal of Zoology 88:1043–1051

[13] FONSECA VS, PETRY MV Y JOST AH (2010) Diet of theMagellanic Penguin on the coast of Rio Grande doSul, Brazil. Waterbirds 24:290–293

[14] FORERO MG, HOBSON KA, BORTOLOTTI GR, DONÁZARJA, BERTELLOTTI M Y BLANCO G (2002) Food resourceutilisation by the Magellanic penguin evaluatedthrough stable-isotope analysis: segregation by sexand age and influence on offspring quality. MarineEcology Progress Series 234:289–299

[15] FRERE E, GANDINI P Y LICHTSCHEIN V (1996) Variaciónlatitudinal en la dieta del pingüino de Magallanes(Spheniscus magellanicus) en la costa patagónica,Argentina. Ornitología Neotropical 7:35–41

[16] FURNESS BL, LAUGKSCH RC Y DUFFY DC (1984)Cephalopods beaks and studies of seabirds diets.Auk 101:619–620

[17] GARCÍA-BORBOROGLU P, BOERSMA PD, RUOPPOLO V,PINHO-DA-SILVA-FILHO R, CORRADO-ADORNES A,CONTE-SENA D, VELOZO R, MYIAJI-KOLESNIKOVAS C,DUTRA G, MARACINI P, CARVALHO-DO-NASCIMENTO C,RAMOS-JÚNIOR V, BARBOSA L Y SERRA S (2010)Magellanic penguin mortality in 2008 along theSW Atlantic coast. Marine Pollution Bulletin60:1652–1657

[18] GONZÁLEZ-SOLÍS J, SMYRLI M, MILITÃO T, GREMILLET D,TYERAA T, PHILLIPS R Y BOULINIER T (2011) Combin-ing stable isotope analyses and geolocation to revealkittiwake migration. Marine Ecology Progress Series435:251–261

[19] HOBSON KA (1999) Tracing origins and migration ofwildlife using stable isotopes: a review. Oecologia120:314–326

[20] HOBSON KA, ALISAUSKAS RT Y CLARK RG (1993) Sta-ble-nitrogen isotope enrichment in avian tissuesdue to fasting and nutritional stress: implicationsfor isotopic analyses of diet. Condor 95:388–394

[21] HOBSON KA Y CLARK RG (1992a) Assessing avian dietsusing stable isotopes I: turnover of 13C in tissues.Condor 94:181–188

[22] HOBSON KA Y CLARK RG (1992b) Assessing avian dietsusing stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197

[23] HOBSON KA, PIATT JF Y PITOCCHELLI J (1994) Using sta-ble isotopes to determine seabird trophic relation-ships. Journal of Animal Ecology 63:786–798INGER R Y BEARHOP S (2008) Applications of stable iso-tope analyses to avian ecology. Ibis 150:447–461

[24] JACKSON AL, INGER R, PARNELL AC Y BEARHOP S (2011)Comparing isotopic niche widths among andwithin communities: SIBER — Stable IsotopeBayesian Ellipses in R. Journal of Animal Ecology80:595–602

[25] JAEGER A, CONNAN P, RICHARD P Y CHEREL Y (2010) Useof stable isotopes to quantify seasonal changes oftrophic niche and levels of population and indi-vidual specialisation in seabirds. Marine EcologyProgress Series 401:269–277

[26] JOBLING M Y BREIBY A (1986) The use and abuse offish otoliths in studies of feeding habits of marinepiscivores. Sarsia 71:265–274

[27] KELLY JF (2000) Stable isotopes of carbon and nitro-gen in the study of avian and mammalian trophicecology. Canadian Journal of Zoology 78:1–27

[28] MÄDER A, SANDER M Y CASA G (2010) Ciclo sazonal demortalidade do influenciado por fatores antrópicose climáticos na costa do Rio Grande do Sul, Brasil.Revista Brasileira de Ornitologia 18:228–233

[29] MARTINEZDEL RÍO C, WOLF S, CARLETON SA Y GANNESLZ (2009) Isotopic ecology ten years after a call formore laboratory experiments. Biological Reviews ofthe Cambridge Philosophical Society 84:91–111

[30] MIZUTANI H, FUKUDA M Y KABAYA Y (1992) 13C and 15Nenrichment factors of feathers of 11 species of adultbirds. Ecology 73:1391–1395

[31] MIZUTANI H, FUKUDA M, KABAYA Y Y WADA E (1990)Carbon isotope ratio of feathers reveals feedingbehavior of cormorants. Auk 107:400–403

[32] NEVES VC, BOLTON M Y MONTEIRO LR (2006) Valida-tion of the water offloading technique for diet as-sessment: an experimental study with Cory ’sshearwaters (Calonectris diomedea). Journal of Orni-thology 147:474–478

[33] PEARSON SF, LAVEY DJ, GREENBERG CH Y MARTÍNEZDELRÍO C (2003) Effects of elemental composition onthe incorporation of dietary nitrogen and carbonisotopic signatures in an omnivorous songbird.Oecologia 135:516–523

[34] PINTO MBLC, SICILIANO S Y DI BENEDITTO APM (2007)Stomach contents of the Magellanic penguinSpheniscus magellanicus from the northern distribu-tion limit on the Atlantic coast of Brazil. MarineOrnithology 35:77–78

[35] PÜTZ K, INGHAM RJ Y SMITH JG (2000) Satellite track-ing of the winter migration of Magellanic PenguinsSpheniscus magellanicus breeding in the FalklandIslands. Ibis 142:614–622

[36] PÜTZ K, SCHIAVINI A, RAYA-REY A Y LUTHI B (2007) Win-ter migration of Magellanic penguins (Spheniscusmagellanicus) from the southernmost distributionalrange. Marine Biology 152:1227–1235

[37] QUILLFELDT P, MCGILL RAR Y FURNESS RW (2005) Dietand foraging areas of Southern Ocean seabirds andtheir prey inferred from stable isotopes: review andcase study of Wilson’s storm-petrel. Marine EcologyProgress Series 295:295–304

[38] RANDALL RM, RANDALL BM Y KLINGELHOEFFER EW(1981) Species diversity and size ranges of cephalo-pods in the diet of Jackass penguins from Algoa Bay,South Africa. South African Journal of Zoology16:163–166

[39] RAYA-REY A, PÜTZ K, SCIOSCIA G, LÜTHI B Y SCHIAVINIA (2012) Sexual differences in the foraging behav-iour of Magellanic Penguins related to stage ofbreeding. Emu 112:90–96

[40] RYAN PG, WILSON RP Y COOPER J (1987) Intraspecificmimicry and status signals in juvenile African pen-guins. Behavioral Ecology and Sociobiology 20:69–76

[41] SCHEINER SM Y GUREVITCH J (2001) Design and analysisof ecological experiments. Segunda edición. OxfordUniversity Press, Oxford

[42] SCHIAVINI A, YORIO P, GANDINI P, RAYA-REY A Y BOERSMAPD (2005) Los pingüinos de las costas argentinas:estado poblacional y conservación. Hornero 20:5–23

[43] SCOLARO JA (1984) Revisión sobre la biología de lareproducción del pingüino de Magallanes. El ciclobiológico anual. Contribuciones Científicas del CentroNacional Patagónico 91:1–26

[44] SCOLARO JA, WILSON R, LAURENTI S, KIERSPEL M,GALLELI H Y UPTON J (1999) Feeding preferences ofthe Magellanic penguin over its breeding range inArgentina. Waterbirds 22:104–110

[45] SILVA L, SAPORITI F, VALES D, TAVARES M, GANDINI P,CRESPO EA Y CARDONA L (2014) Differences in dietcomposition and foraging patterns between sexesof the Magellanic penguin (Spheniscus magellanicus)during the non-breeding period as revealed by δ13Cand δ15N values in feathers and bone. Marine Biol-ogy 161:1195–1206

[46] THOMPSON DR, FURNESS RW Y LEWIS SA (1995) Dietsand long-term changes in δ15N and δ13C values innorthern fulmars Fulmarus glacialis from two north-east Atlantic colonies. Marine Ecology Progress Series125:3–11

[47] TIESZEN LL, BOUTTON TW, TESDAHL KG Y SLADE NA(1983) Fractionation and turnover of stable carbonisotopes in animal tissues: implications for δ13Canalysis of diet. Oecologia 57:32–37

[48] WILSON RP, LA COCK GD, WILSON MP Y MOLLAGEE F(1985) Differential digestion of fish and squid inJackass Penguins Spheniscus demersus. Ornis Scandi-navica 16:77–79

[49] WILSON RP, MANDY A, KIERSPEL M, SCOLARO A,LAURENTI S, UPTON J, GALLELLI H, FRERE E Y GANDINIP (1999) To think or swim: does it really cost pen-guins more to waddle? Journal of Avian Biology30:221–224

[50] WILSON RP, SCOLARO JA, GRÉMILLET D, KIERSPEL MAM,LAURENTI S, UPTON J, GALLELLI H, QUINTANA F, FREREE Y MÜLLER G (2005) How do Magellanic Penguinscope with variability in their access to prey? Eco-logical Monographs 75:379–401