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Holocene changes in the trophic ecology of an apex marine predator in the South Atlantic Ocean


Predators may modify their diets as a result of both anthropogenic and natural environmental changes. Stable isotope ratios of nitrogen and carbon in bone collagen have been used to reconstruct the foraging ecology of South American fur seals (Arctocephalus australis) in the southwestern South Atlantic Ocean since the Middle Holocene, a region inhabited by hunter-gatherers by millennia and modified by two centuries of whaling, sealing and fishing. Results suggest that the isotopic niche of fur seals from Patagonia has not changed over the last two millennia (average for the period: δ13C2200-0BP = −13.4 ± 0.5‰, δ15N2200-0BP = 20.6 ± 1.1‰). Conversely, Middle Holocene fur seals fed more pelagically than their modern conspecifics in the Río de la Plata region (δ13C7000BP = −15.9 ± 0.6‰ vs. δ13CPRESENT = −13.5 ± 0.8‰) and Tierra del Fuego (δ13C6400-4300BP = −15.4 ± 0.5‰ vs. δ13CPRESENT = −13.2 ± 0.7‰). In the latter region, Middle Holocene fur seals also fed at a higher trophic level than their modern counterparts (δ15N6400-4300BP = 20.5 ± 0.5‰ vs. δ15NPRESENT = 19.0 ± 1.6‰). Nevertheless, a major dietary shift was observed in fur seals from Tierra del Fuego during the nineteenth century (δ13C100BP = −17.2 ± 0.3‰, δ15N100BP = 18.6 ± 0.7‰), when marine primary productivity plummeted and the fur seal population was decimated by sealing. Disentangling the relative roles of natural and anthropogenic factors in explaining this dietary shift is difficult, but certainly the trophic position of fur seals has changed through the Holocene in some South Atlantic regions.

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  1. Acha EM, Guerrero R, Favero M, Bava J (2004) Marine fronts at the continental shelves of austral South America: physical and ecological processes. J Mar Syst 44:83–105. doi:10.1016/j.jmarsys.2003.09.005

  2. Aguirre ML (1993) Palaeobiogeography of the Holocene molluscan fauna from Northeastern Buenos Aires Province, Argentina: its relation to coastal evolution and sea level changes. Palaeogeogr Palaeoclimatol Palaeoecol 102:1–26. doi:10.1016/0031-0182(93)90002-Z

  3. Aguirre ML, Donato M, Richiano S, Farinati EA (2011) Pleistocene and Holocene interglacial molluscan assemblages from Patagonian and Bonaerensian littoral (Argentina, SW Atlantic): palaeobiodiversity and palaeobiogeography. Palaeogeogr Palaeoclimatol Palaeoecol 308:277–292. doi:10.1016/j.palaeo.2011.05.032

  4. Aldazabal V, Eugenio E, Silveira M (2011) Arqueología del sector costero al sur de Bahía de San Blas: sitio las Olas 11. Rev Estud Marit Soc 4:1–19

  5. Balech E, Ehrlich MD (2008) Esquema biogeográfico del Mar Argentino. Rev Invest Desarr Pesq 19:45–75

  6. Baylis AMM, Arnould JPY, Staniland IJ (2014) Diet of fur seals at the Falkland Islands. Mar Mammal Sci 30:1210–1219. doi:10.1111/mms.12090

  7. Baylis AMM, Orben RA, Arnould JPY, Christiansen F, Hays GC, Staniland IJ (2015) Disentangling the cause of a catastrophic population decline in a large marine mammal. Ecology 96:2834–2847. doi:10.1890/14-1948.1

  8. Bayón MC, Politis GG (1996) Estado actual de las investigaciones en el sitio Monte Hermoso 1, Provincia de Buenos Aires. Arqueol (Instituto de Arqueología FFyL UBA) 6:83–116

  9. Bayón MC, Politis GG (2014) The inter-tidal zone Site of La Olla: early–Middle Holocene human adaptation on the Pampean coast of Argentina. In: Evans AM, Flatman JC, Flemming NC (eds) Prehistoric archaeology on the continental shelf: a global review. Springer, New York, pp 115–130. doi:10.1007/978-1-4614-9635-9_7

  10. Bayón C, Frontini R, Vecchi R (2012) Middle Holocene settlements on coastal dunes, southwest Buenos Aires Province, Argentina. Quat Int 256:54–61. doi:10.1016/j.quaint.2011.07.014

  11. Beretta M, Corinaldessi L, Castro A (2011) Recursos marinos vs. recursos terrestres: análisis arqueofaunístico en el sitio Cueva del Negro, costa norte de Santa Cruz. Arqueol (Inst de Arqueol FFyL UBA) 17:137–159

  12. Blasi A, Politis G, Bayón C (2013) Palaeoenvironmental reconstruction of La Olla, a Holocene archaeological site in the Pampean coast (Argentina). J Archaeol Sci 40:1554–1567. doi:10.1016/j.jas.2012.09.016

  13. Bligh E, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917. doi:10.1139/o59-099

  14. Bonner WN (1982) Seals and man. A study of interactions. University of Washington Press, Seattle

  15. Bonomo M (2005) Costeando las llanuras. Arqueología del litoral marítimo pampeano. Colección Tesis de Doctorado, Sociedad Argentina de Antropología, Buenos Aires

  16. Bonomo M (2011) The use of the space in the Pampean Atlantic coast and the adjacent plains (Argentina, South America): a comparative view. In: Bicho NF, Haws JA, Davis LG (eds) Trekking the shore: changing coastlines and the antiquity of coastal settlement. Springer, New York, pp 333–353. doi:10.1007/978-1-4419-8219-3_14

  17. Bonomo M, León C (2010) Un contexto arqueológico en posición estratigráfica en los médanos litorales. El sitio Alfar (pdo. Gral. Pueyrredón, Pcia. Bs. As.). In: Berón M, Luna L, Bonomo M, Montalvo C, Aranda C, Aizpitarte M (eds) Mamül Mapu: pasado y presente desde la arqueología pampeana. Ayacucho, Del Espinillo, pp 29–45

  18. Bonomo M, Scabuzzo C, León DC (2013) Cronología y dieta en la costa atlántica pampeana, Argentina. Intersecciones Antropol 14:123–136

  19. Borella F (2014) Zooarchaeological evidence of Otariids in continental coast of Patagonia, Argentina: Old and new perspectives. In: Muñoz AS, Götz CM, Roca ER (eds) Neotropical and Caribbean aquatic mammals. Perspectives from archaeology and conservation biology. Nova Science Publishers, New York, pp 135–160

  20. Borella F, Cruz I (2012) Taphonomic evaluation of penguin (Spheniscidae) remains at a shell-midden on the northern coast of Patagonia (San Matías Gulf, Río Negro, Argentina). Quat Int 278:45–50. doi:10.1016/j.quaint.2012.04.023

  21. Boretto GM, Gordillo S, Cioccale M, Colombo F, Fucks E (2013) Multi-proxy evidence of Late Quaternary environmental changes in the coastal area of Puerto Lobos (northern Patagonia, Argentina). Quat Int 305:188–205. doi:10.1016/j.quaint.2013.02.017

  22. Bugoni L, McGill RAR, Furness RW (2010) The importance of pelagic longline fishery discards for a seabird community determined through stable isotope analysis. J Exp Mar Biol Ecol 391:190–200. doi:10.1016/j.jembe.2010.06.027

  23. Bunn SE, Loneragan NR, Kempster MA (1995) Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: implications for food-web studies using multiple stable isotopes. Limnol Oceanogr 40:622–625. doi:10.4319/lo.1995.40.3.0622

  24. Burton RK, Snodgrass JJ, Gifford-Gonzalez D, Guilderson T, Brown T, Koch PL (2001) Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna. Oecologia 128:107–115. doi:10.1007/s004420100631

  25. Burton RK, Gifford- Gonzalez D, Snodgrass JJ, Koch PL (2002) Isotopic tracking of prehistoric pinniped foraging and distribution along the Central California Coast: preliminary results. Int J Osteoarchaeol 12:4–11. doi:10.1002/oa.608

  26. Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. P Natl Acad Sci USA 93:10844–10847

  27. Casey MM, Post DM (2011) The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth-Sci Rev 106:131–148. doi:10.1016/j.earscirev.2011.02.001

  28. Castilho PV, Simões-Lopes PC (2008) Sea mammals in archaeological sites on the southern coast of Brazil. Rev Mus Arqueol Etnol, São Paulo 18:101–113

  29. Ciancio JE, Pascual M, Botto F, Frere E, Iribarne O (2008) Trophic relationships of exotic anadromous salmonids in the Southern Patagonian Shelf as inferred from stable isotopes. Limnol Oceanogr 53:788–798. doi:10.4319/lo.2008.53.2.0788

  30. Clark AH (1887) The Antarctic fur-seal and sea-elephant Industries. In: Goode GB (ed) The fisheries and fishery industries of the Unites States. Section V, history and methods of the fisheries, vol 2. Government Printing Office, Washington, pp 400–467

  31. Codignotto JO, Aguirre ML (1993) Coastal evolution, changes in sea level and molluscan fauna in northeastern Argentina during the Late Quaternary. Mar Geol 110:163–175. doi:10.1016/0025-3227(93)90112-9

  32. Cousseau MB, Perrota RG (2004) Peces marinos de Argentina. Biología, distribución, pesca, 3ra edn. Publicaciones Especiales INIDEP, Mar del Plata

  33. Crespo EA, Schiavini ACM, García NA, Franco Trecu V, Goodall RNP, Rodríguez D, Morgante JS, Oliveira LR (2015) Status, population trend and genetic structure of South American fur seals Arctocephalus australis in southwestern Atlantic waters. Mar Mammal Sci 31:866–890. doi:10.1111/mms.12199

  34. DeNiro MJ (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317:806–809. doi:10.1038/317806a0

  35. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Ac 42:495–506. doi:10.1016/0016-7037(78)90199-0

  36. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Ac 45:341–351. doi:10.1016/0016-7037(81)90244-1

  37. Dickinson AB (2007) Seal fisheries of the Falkland Islands and dependencies: an historical overview (Research in maritime History No. 34). Marquis Book Printing Inc., St John’s, Newfoundland

  38. Drago M, Crespo EA, Aguilar A, Cardona L, García N, Dans SL, Goodall N (2009) Historic diet change of the South American sea lion in Patagonia as revealed by isotopic analysis. Mar Ecol Prog Ser 384:273–286. doi:10.3354/meps08017

  39. Drago M, Cardona L, Crespo EA, Grandi MF, Aguilar A (2010) Reduction of skull size in South American sea lions reveals density-dependent growth during population recovery. Mar Ecol Prog Ser 420:253–261. doi:10.3354/meps08887

  40. Erlandson JM, Rick TC (2008) Archaeology, marine ecology, and human impacts on marine environments. In: Rick TC, Erlandson JM (eds) Human impacts on ancient marine ecosystems: a global perspective. University of California Press, Berkeley, pp 1–20

  41. Etnier M (2004) Reevaluating evidence of density-dependent growth in northern fur seals (Callorhinus ursinus) based on measurements of archived skeletal specimens. Can J Fish Aquat Sci 61:1616–1626. doi:10.1139/f04-090

  42. Eugenio E, Aldazabal V (2004) Los cazadores recolectores del litoral marítimo del área de Bahía de San Blas, provincia de Buenos Aires. Civalero MT, Fernández P, Guráieb G (comp) Contra viento y marea. Arqueología de Patagonia. Instituto Nacional de Antropología y Pensamiento Latinoamericano, Buenos Aires, pp 687–700

  43. Favier Dubois CM, Borella F, Tykot RH (2009) Explorando tendencias en el uso humano del espacio y los recursos en el litoral rionegrino durante el Holoceno tardío y medio. In: Salemme M, Santiago F, Álvarez M, Piana E, Vázquez M, Mansur E (eds) Arqueología de Patagonia: una mirada desde el último confín. Utopías, Ushuaia, pp 985–997

  44. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:307–312. doi:10.3354/meps124307

  45. Franco-Trecu V, Aurioles-Gamboa D, Inchausti P (2014) Individual trophic specialisation and niche segregation explain the contrasting population trends of two sympatric otariids. Mar Biol 161:609–618. doi:10.1007/s00227-013-2363-9

  46. Gómez Otero J (2007a) Dieta, uso del espacio y evolución en sociedades cazadoras-recolectoras de la costa centro-septentrional de Patagonia durante el Holoceno medio y tardío. PhD dissertation, Universidad de Buenos Aires, Buenos Aires

  47. Gómez Otero J (2007b) Isótopos estables, dieta y uso del espacio en la costa atlántica centro-septentrional y el valle inferior del río Chubut (Patagonia, Argentina. In: Morello F, Martinic M, Prieto A, Bahamond G (eds) Arqueología de Fuego-Patagonia. Levantando piedras, desenterrando huesos, y develando arcanos. CEQUA, Punta Arenas, pp 151–161

  48. Grupe G, Piepenbrink H (1987) Processing of prehistoric bones for isotopic analysis and the meaning of collagen C/N ratios in the assessment of diagenetic effects. Hum Evol 2:511–515. doi:10.1007/BF02437425

  49. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi:10.1126/science.1149345

  50. Hanson NN, Wurster CM, Bird MI, Reid K, Boyd IL (2009) Intrinsic and extrinsic forcing in life histories: patterns of growth and stable isotopes in male Antarctic fur seal teeth. Mar Ecol Prog Ser 388:263–272. doi:10.3354/meps08158

  51. Hirons AC, Schell DM, Finney BP (2001) Temporal records of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diet. Oecologia 129:591–601. doi:10.1007/s004420100756

  52. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798. doi:10.2307/5256

  53. Inda H, Puerto L, Castiñeira C, Capdepont I, García-Rodríguez F (2006) Aprovechamiento prehistórico de recursos costeros en el litoral atlántico uruguayo. In: Menafra R, Rodríguez-Gallego L, Scarabino F, Conde D (eds) Bases para la conservación y el manejo de la costa uruguaya. Vida Silvestre Uruguay, Montevideo, pp 661–667

  54. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638. doi:10.1126/science.1059199

  55. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: sIBER–Stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602. doi:10.1111/j.1365-2656.2011.01806.x

  56. Keeling CD (1979) The Suess effect: 13Carbon-14Carbon interrelations. Environ Int 2:229–300. doi:10.1016/0160-4120(79)90005-9

  57. Koen Alonso M, Yodzis P (2005) Multispecies modelling of some components of the marine community of northern and central Patagonia, Argentina. Can J Fish Aquat Sci 62:1490–1512. doi:10.1139/F05-087

  58. León DC (2014) Zooarqueología de cazadores-recolectores del Litoral Pampeano: Un enfoque multidimensional. PhD dissertation, Universidad Nacional del Centro, Buenos Aires

  59. Lorrain A, Savoye N, Chauvaud L, Paulet Y, Naulet N (2003) Decarbonation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material. Anal Chim Acta 491:125–133. doi:10.1016/S0003-2670(03)00815-8

  60. Lotze HK, Worm B (2009) Historical baselines for large marine animals. Trends Ecol Evol 24:254–262. doi:10.1016/j.tree.2008.12.004

  61. McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol Oceanogr 58:697–714. doi:10.4319/lo.2013.58.2.0697

  62. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Ac 48:1135–1140. doi:10.1016/0016-7037(84)90204-7

  63. Misarti N, Finney B, Maschner H, Wooller MJ (2009) Changes in northeast Pacific marine ecosystems over the last 4500 years: evidence from stable isotope analysis of bone collagen from archeological middens. Holocene 19:1139–1151. doi:10.1177/0959683609345075

  64. Moreno E (2008) Arqueología y etnohistoria de la costa patagónica central en el Holoceno tardío. Fondo Editorial Provincial-Secretaría de Cultura del Chubut, Rawson

  65. Moreno E, Zangrando AF, Tessone A, Castro A, Panarello H (2011) Isótopos estables, fauna y tecnología en el estudio de los cazadores-recolectores de la costa norte de Santa Cruz. Magallania (Punta Arenas) 39:265–276. doi:10.4067/S0718-22442011000100017

  66. Muñoz AS (2011) Pinniped zooarchaeological studies in Southern Patagonia: current issues and future research agenda. In: Bicho NF, Haws JA, Davis LG (eds) Trekking the shore: changing coastlines and the antiquity of coastal settlement. Springer, New York, pp 305–331. doi:10.1007/978-1-4419-8219-3_13

  67. Nagai RH, Sousa SHM, Lourenço RA, Bícego MC, Mahiques MM (2010) Paleoproductivity changes during the Late Quaternary in the Southeastern Brazilian upper continental margin of the Southwestern Atlantic. Braz J Oceanogr 58:31–41. doi:10.1590/S1679-87592010000500004

  68. Naya DE, Arim M, Vargas R (2002) Diet of South American fur seals (Arctocephalus australis) in Isla de Lobos, Uruguay. Mar Mammal Sci 18:734–745. doi:10.1111/j.1748-7692.2002.tb01070.x

  69. Newsome SD, Koch P, Etnier M, Aurioles-Gamboa D (2006) Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Mar Mammal Sci 22:556–572. doi:10.1111/j.1748-7692.2006.00043.x

  70. Newsome SD, Etnier MA, Gifford-Gonzalez D, Phillips DL, van Tuinen M, Hadly EA, Costa DP, Kennett DJ, Guilderson TP, Koch PL (2007a) The shifting baseline of northern fur seal ecology in the northeast Pacific Ocean. P Natl Acad Sci USA 104:9709–9714. doi:10.1073/pnas.0610986104

  71. Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007b) A niche for isotopic ecology. Front Ecol Environ 5:429–436. doi:10.1890/060150.1

  72. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mammal Sci 26:509–572. doi:10.1111/j.1748-7692.2009.00354.x

  73. Oliveira LR (2004) Variaçao geográfica do lobo-marinho sul-americano, Arctocephalus australis (Zimmermann, 1783) com base em dados morfológicos e moleculares. PhD dissertation, Universidade de São Paulo, São Paulo

  74. Oliveira LR, Ott PH, Malbarba LR (2008a) Ecologia alimentar dos pinípedes do sul do Brasil e uma avaliação de suas interações com atividades pesqueiras. In: Reis NRd, Peracchi AL, Dos Santos GASD (eds) Ecologia de Mamíferos. Technical Books Editora, Londrina, pp 97–116

  75. Oliveira LR, Hoffman JI, Hingst-Zaher E, Majluf P, Muelbert MMC, Morgante JS, Amos W (2008b) Morphological and genetic evidence for two evolutionarily significant units (ESUS) in the South American fur seal, Arctocephalus australis. Conserv Genet 9:1451–1466. doi:10.1007/s10592-007-9473-1

  76. Orquera LA (2002) The late-nineteenth century crisis in the survival of the Magellan-Fueguian littoral natives. In: Briones C, Lanata JL (eds) Archaeological and anthropological perspectives on the native peoples of Pampa, Patagonia, and Tierra del Fuego to the nineteenth century. Bergin and Garvey, Westport, pp 145–158

  77. Orquera LA, Gómez Otero J (2007) Los cazadores-recolectores de las costas de Pampa, Patagonia y Tierra del Fuego. Relac Soc Argent Antropol 32:75–99

  78. Orquera LA, Piana EL (1996) El sitio Shamakush 1 (Tierra del Fuego, República Argentina). Relac Soc Argent Antropol 21:215–265

  79. Orquera LA, Piana EL (1999) Arqueología de la región del canal Beagle (Tierra del Fuego, República Argentina). Sociedad Argentina de Antropología, Buenos Aires

  80. Orquera LA, Piana EL (2000) Imiwaia I: un sitio de canoeros del sexto milenio A.P. en la costa norte del canal Beagle. In: Belardi JB, Carballo Marina F, Espinosa S (eds) Desde el país de los gigantes. Perspectivas arqueológicas en Patagonia, Tomo II. Universidad Nacional de la Patagonia Austral, Río Gallegos, pp 441–453

  81. Pinnegar JK, Engelhard GH (2008) The ‘shifting baseline’ phenomenon: a global perspective. Rev Fish Biol Fisheries 18:1–16. doi:10.1007/s11160-007-9058-6

  82. Ponce JF, Rabassa R, Coronato A, Borromei AM (2011) Paleogeographic evolution of the Atlantic coast of Pampa and Patagonia since the last glacial maximum to the Middle Holocene. Biol J Linn Soc 103:363–379. doi:10.1111/j.1095-8312.2011.01653.x

  83. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. doi:10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2

  84. Sánchez RP, de Ciechomski JD (1995) Spawning and nursery grounds of pelagic fish species in the sea-shelf off Argentina and adjacent areas. Sci Mar 59:455–478

  85. Saporiti F, Bala LO, Crespo EA, Gómez Otero J, Zangrando AFJ, Aguilar A, Cardona L (2013) Changing patterns of marine resource exploitation by hunter-gatherers throughout the late Holocene of Argentina are uncorrelated to sea surface temperature. Quat Int 299:108–115. doi:10.1016/j.quaint.2013.03.026

  86. Saporiti F, Bearhop S, Silva L, Vales DG, Zenteno L, Crespo EA, Aguilar A, Cardona L (2014a) Longer and less overlapping food webs in anthropogenically disturbed marine ecosystems: confirmations from the past. PLoS One 9:e103132. doi:10.1371/journal.pone.0103132

  87. Saporiti F, Bala LO, Gómez Otero J, Crespo EA, Piana EL, Aguilar A, Cardona L (2014b) Paleoindian pinniped exploitation in South America was driven by oceanic productivity. Quat Int 352:85–91. doi:10.1016/j.quaint.2014.05.015

  88. Saporiti F, Bearhop S, Vales DG, Silva L (2015) Latitudinal changes in the structure of marine food webs in the Southwestern Atlantic Ocean. Mar Ecol Prog Ser 538:23–34. doi:10.3354/meps11464

  89. Scheffer VB (1955) Body size with relation to population density in mammals. J Mammal 36:493–515. doi:10.2307/1375805

  90. Schiavini ACM (1992) Hombres y lobos marinos en la Sudamérica Austral. In: Lichter AA (ed) Huellas en la arena, sombras en el mar. Los mamíferos marinos de la Argentina y la Antártida, Ediciones Terra Nova, Buenos Aires, pp 250–254

  91. Schiavini ACM (1993) Los lobos marinos como recurso para cazadores-recolectores marinos: el caso de Tierra del Fuego. Lat Am Antiq 4:346–366. doi:10.2307/972072

  92. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochim Ac 48:625–639. doi:10.1016/0016-7037(84)90091-7

  93. Strange IJ (1983) The Falkland Islands, 3rd edn. David and Charles, London

  94. Strange IJ (1992) A field guide to the wildlife of the Falkland Islands and South Georgia. Harper and Collins, London

  95. Tivoli A, Zangrando AF (2011) Subsistence variations and landscape use among maritime hunter-gatherers. A zooarchaeological analysis from the Beagle Channel (Tierra del Fuego, Argentina). J Archaeol Sci 38:1148–1156. doi:10.1016/j.jas.2010.12.018

  96. Toledo FAL, Costa KB, Pivel MAG, Campos EJD (2008) Tracing past circulation changes in the Western South Atlantic based on planktonic foraminifera. Rev Bras Paleontol 11:169–178. doi:10.4072/rbp.2008.3.03

  97. Townsend CH (1910) Fur seals and the seal fisheries. In: Bumpus HC, Smith HM (eds) Proceeding of the fourth International fishery congress: organization and sessional business, papers and discussions. Held at Washington, U.S.A., September 22–26, 1908 (Bulletin of the Bureau of Fisheries 28). Government Printing Office, Washington, pp 315–322

  98. Trites AW, Bigg MA (1992) Changes in body growth of northern fur seals from 1958 to 1974: density effects or changes in the ecosystem? Fish Oceanogr 1:127–136. doi:10.1111/j.1365-2419.1992.tb00031.x

  99. Vales DG (2015) Uso actual y pasado de los recursos tróficos por parte del lobo marino de dos pelos Arctocephalus australis (Zimmermann, 1783) en el Océano Atlántico Sudoccidental. PhD dissertation, Universidad Nacional de Mar del Plata, Mar del Plata

  100. Vales DG, Saporiti F, Cardona L, Oliveira LR, dos Santos RA, Secchi ER, Aguilar A, Crespo EA (2014) Intensive fishing has not forced dietary change in the South American fur seal Arctophoca (=Arctocephalus) australis off Río de la Plata and adjoining areas. Aquatic Conserv Mar Freshw Ecosyst 24:745–759. doi:10.1002/aqc.2397

  101. Vales DG, Cardona L, García NA, Zenteno L, Crespo EA (2015) Ontogenetic dietary changes in male South American fur seals Arctocephalus australis in Patagonia. Mar Ecol Prog Ser 525:245–260. doi:10.3354/meps11214

  102. Van Klinken GJ (1999) Bone collagen quality indicators for palaeodietary and radiocarbon measurements. J Archaeol Sci 26:687–695. doi:10.1006/jasc.1998.0385

  103. Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404. doi:10.1890/0012-9658(1999)080[1395:PCCANA]2.0.CO;2

  104. Zangrando AF (2009) Historia evolutiva y subsistencia de cazadores-recolectores marítimos de Tierra del Fuego. Colección Tesis de Doctorado, Sociedad Argentina de Antropología, Buenos Aires

  105. Zangrando AF, Orquera LA, Piana EL (2010) Diversificación e intensificación de recursos animales en la secuencia arqueológica del canal Beagle (Tierra del Fuego, Argentina). In: Gutiérrez MA, De Nigris M, Fernández PM, Giardina M, Gil AF, Izeta A, Neme G, Yacobaccio HD (eds) Zooarqueología a principios del siglo XXI: aportes teóricos, metodológicos y casos de estudio. Ediciones del Espinillo, Buenos Aires, pp 359–370

  106. Zangrando AF, Panarello H, Piana EL (2014) Zooarchaeological and stable isotopic assessments on pinniped—human relations in the Beagle channel (Tierra del Fuego, Southern South America). Int J Osteoarchaeol 24:231–244. doi:10.1002/oa.2352

  107. Zenteno L, Borella F, Otero JG, Piana E, Belardi JB, Borrero LA, Saporiti F, Cardona L, Crespo E (2015) Shifting niches of marine predators due to human exploitation: the diet of the South American sea lion (Otaria flavescens) since the late Holocene as a case study. Paleobiology 41:387–401. doi:10.1017/pab.2015.9

  108. Zubimendi MA, Ambrústolo P, Beretta M, Mazzitelli L, Hammond H, Zilio L, Ciampagna L, Trola V, Plischuk M, Castro AS (2011) Sitio Cueva del Negro: un caso de aprovechamiento intensivo de los recursos marinos en la costa norte de Santa Cruz (Patagonia argentina). Rev Estud Marit Soc 4:51–62

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This article is dedicated to the memory of R. Natalie P. Goodall, deceased during the preparation of the manuscript. Archaeological samples from La Olla 1 and Barrio Las Dunas sites were kindly provided by Gustavo Politis (INCUAPA-UNCPBA-CONICET and the Universidad Nacional de La Plata) and Cristina Bayón (Universidad Nacional del Sur, Bahía Blanca), whereas archaeological remains from northern and central Patagonia sites were kindly supplied by Julieta Gómez Otero and Eduardo Moreno (IDEAus-CCT CONICET-CENPAT). Modern samples of fur seals from Brazil were collected and provided by the members of Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS). The authors would like to thank the three anonymous reviewers for their valuable comments and suggestions that helped greatly to improve the manuscript. We also thank Ross Barnett (University of Copenhagen, Centre for GeoGenetics, Geologic Museum) for reviewing the English language of the manuscript. The map presented in this paper is courtesy of SEATURTLE.ORG (information is available at This research article is part of the PhD thesis of D.G.V. At the time this manuscript was written, D.G.V. was supported by the Fellowship Program from the National Research Council of Argentina (CONICET) and F.S. was supported by a Fellowship from the Ministerio de Ciencia e Innovación (Spain). This research was funded by Fundación BBVA through the project “Efectos de la explotación humana sobre depredadores apicales y la estructura de la red trófica del Mar Argentino durante los últimos 6.000 años” (BIOCON 08-194/09 2009-2011); Agencia Nacional de Promoción Científica y Tecnológica (PICT No 2110) and the Zoo d’Amneville, France.

Author contribution statement

DGV, LC and EAC conceived and designed the experiments. DGV, AFZ, FB, FS, RNPG, LRO and EAC conducted fieldwork. DGV, AFZ and FS performed the experiments. DGV, LC and FS analysed the data. DGV and LC wrote the manuscript, with contributions from all authors.

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Correspondence to Damián G. Vales.

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Additional information

R. Natalie P. Goodall: deceased.

Communicated by Helene Marsh.

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Vales, D.G., Cardona, L., Zangrando, A.F. et al. Holocene changes in the trophic ecology of an apex marine predator in the South Atlantic Ocean. Oecologia 183, 555–570 (2017).

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  • Fur seals
  • Arctocephalus australis
  • Historical ecology
  • Hunter-gatherers
  • Sealing
  • Environmental changes
  • Stable isotopes