Marine Biology

, 164:86 | Cite as

Trophic structure in the northern Humboldt Current system: new perspectives from stable isotope analysis

  • Pepe Espinoza
  • Anne LorrainEmail author
  • Frédéric Ménard
  • Yves Cherel
  • Laura Tremblay-Boyer
  • Juan Argüelles
  • Ricardo Tafur
  • Sophie Bertrand
  • Yann Tremblay
  • Patricia Ayón
  • J.-M. Munaron
  • Pierre Richard
  • Arnaud Bertrand
Original Paper


The northern Humboldt Current system (NHCS) is the most productive eastern boundary upwelling system (EBUS) in terms of fish productivity despite having a moderate primary production compared with other EBUS. To understand this apparent paradox, an updated vision of the trophic relationships in the NHCS is required. Using δ13C and δ15N as a proxy of foraging habitat and trophic position, respectively, we focused on thirteen relevant taxonomic groups from zooplankton to air-breathing top predators collected off Peru from 2008 to 2011. Estimates of trophic position (TP) for the anchoveta Engraulis ringens were high (3.4–3.7), in accordance with previous studies showing zooplankton as a major contributor to anchoveta diet and challenging the often-cited short food chain hypothesis for this ecosystem. The squat lobster, Pleuroncodes monodon, a little studied consumer had similar δ15N values that of anchoveta, and thus similar trophic position. However, their differing δ13C values indicate that their foraging habitat do not fully overlap, which could alleviate potential competition between these species. Given the current high biomass of squat lobsters in the ecosystem, we encourage that future research focus on this species and its role in the diet of top predators. The present study provides first estimates of the relative TP of important taxonomic groups in the NHCS, which are needed to revisit anchoveta-centred ecosystem models for this region. Further work using amino acid compound specific stable isotope analyses is now required to confirm these TP estimates.


Anammox Trophic Position Discrimination Factor Jack Mackerel Mesopelagic Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work is a contribution to the cooperative agreement between the Instituto del Mar del Peru (IMARPE), the Institut de Recherche pour le Developpement (IRD), and of the LMI DISCOH. This publication was made possible through support provided by the ANR TOPINEME. We would like to thank G. Guillou from the LIENSs laboratory for stable isotope analysis, and the two anonymous reviewers for their constructive comments on the manuscript. PE was financially supported by the BEST Grant from IRD and managed by Campus France.

Compliance with ethical standards

This study was funded by IRD, IMARPE and ANR TOPINEME. None of the coauthors have ethical issues arising from conflicts of interest. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2017_3119_MOESM1_ESM.pdf (78 kb)
Supplementary material 1 (PDF 78 KB)


  1. Alegre A, Ménard F, Tafur R, Espinoza P, Argüelles J, Maehara V, Simer M, Bertrand A (2014) Comprehensive model of jumbo squid Dosidicus gigas trophic ecology in the northern Humboldt Current system. PLoS ONE 9:e85919. doi: 10.1371/journal.pone.0085919 CrossRefGoogle Scholar
  2. Alegre A, Bertrand A, Espino M, Espinoza P, Dioses T, Ñiquen M, Navarro I, Simier M, Ménard F (2015) Diet diversity of jack and chub mackerels and ecosystem changes in the northern Humboldt Current system: a long-term study. Progr Oceanogr 137:299–313. doi: 10.1016/j.pocean.2015.07.010
  3. Angelescu V (1982) Ecología trófica de la anchoita del mar argentino (Engraulidae, Engraulis anchoita). Parte II. Alimentación, comportamiento y relaciones tróficas en el ecosistema. Contribución INIDEP 409:83Google Scholar
  4. Argüelles J, Lorrain A, Cherel Y, Graco M, Tafur R, Alegre A, Espinoza P, Taipe A, Ayón P, Bertrand A (2012) Tracking habitat and resource use for the jumbo squid Dosidicus gigas: a stable isotope analysis in the Northern Humboldt Current System. Mar Biol 159:2105–2116. doi: 10.1007/s00227-012-1998-2 CrossRefGoogle Scholar
  5. Arias-Schereiber M (1996) Informe sobre el estado de conocimientos y conservación de los mamíferos marinos en el Perú. Inf Progr Inst Mar Perú 38, pp 30Google Scholar
  6. Armstrong MJ, James AG, Valdés Szeinfeld ES (1991) Estimates of annual consumption of food by anchovy and other pelagic fish species off South Africa during the period 1984–1988. S Afr J Marine Sci 11:251–266. doi: 10.2989/025776191784287781
  7. Ayón P, Swartzman G, Bertrand A, Gutiérrez M, Bertrand S (2008a) Zooplankton and forage fish species off Peru: Large-scale bottom-up forcing and local-scale depletion. Progr Oceanogr 79:208–214. doi: 10.1016/j.pocean.2008.10.023
  8. Ayón P, Criales-Hernandez MI, Schwamborn R, Hirche HJ (2008b) Zooplankton research off Peru: a review. Progr Oceanogr 79:238–255. doi: 10.1016/j.pocean.2008.10.020
  9. Bakun A, Weeks SJ (2008) The marine ecosystem off Peru: What are the secrets of its fishery productivity and what might its future hold? 79:290–299. doi: 10.1016/j.pocean.2008.10.027
  10. Barber RT, Chavez FP (1983) Biological consequences of El Niño. Science 222:1203–1210. doi: 10.1126/science.222.4629.1203 CrossRefGoogle Scholar
  11. Bertrand A, Gerlotto F, Bertrand S, Gutiérrez M, Alza L, Chipollini A, Díaz E, Espinoza P, Ledesma J, Quesquén R, Peraltilla S, Chavez F (2008a) Schooling behaviour and environmental forcing in relation to anchoveta distribution: An analysis across multiple spatial scales. Progr Oceanogr 79:264–277. doi: 10.1016/j.pocean.2008.10.018
  12. Bertrand S, Dewitte B, Tam J, Díaz E, Bertrand A (2008b) Impacts of Kelvin wave forcing in the Peru Humboldt Current system: scenarios of spatial reorganizations from physics to fishers. Progr Oceanogr 79:278–289. doi: 10.1016/j.pocean.2008.10.017
  13. Bertrand A, Ballón M, Chaigneau A (2010) Acoustic observation of living organisms reveals the upper limit of the oxygen minimum zone. PLoS One 5(4):e10330. doi: 10.1371/journal.pone.0010330 CrossRefGoogle Scholar
  14. Bertrand A, Chaigneau A, Peraltilla S, Ledesma J, Graco M, Monetti F, Chavez FP (2011) Oxygen: a fundamental property regulating pelagic ecosystem structure in the coastal southeastern tropical Pacific. PLoS ONE 6(12):e29558. doi: 10.1371/journal.pone.0029558 CrossRefGoogle Scholar
  15. Bertrand A, Grados D, Colas F, Bertrand S, Capet X, Chaigneau A, Vargas G, Mousseigne A, Fablet R (2014) Broad impacts of fine-scale dynamics on seascape structure from zooplankton to seabirds. Nat Commun 5:5239. doi: 10.1038/ncomms6239 CrossRefGoogle Scholar
  16. Bode A, Alvarez-Ossorio MT, Cunha ME, Garrido S, Peleteiro JB, Porteiro C, Valdés L, Varela M (2007) Stable nitrogen isotope studies of the pelagic food web on the Atlantic shelf of the Iberian Peninsula. Progr Oceanogr 74:115–131. doi: 10.1016/j.pocean.2007.04.005
  17. Boyd CM, Smith SL, Cowles TJ (1980) Grazing patterns of copepods in the upwelling system off Peru. Limnol Oceanogr 25:583–596. doi: 10.4319/lo.1980.25.4.0583 CrossRefGoogle Scholar
  18. Brochier T, Lett C, Fréon P (2011) Investigating the ‘northern Humboldt paradox’ from model comparisons of small pelagic fish reproductive strategies in eastern boundary upwelling ecosystems. Fish Fish 12:94–109. doi: 10.1111/j.1467-2979.2010.00385.x CrossRefGoogle Scholar
  19. Bugoni L, Mcgill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462. doi: 10.1002/rcm.3633 CrossRefGoogle Scholar
  20. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453CrossRefGoogle Scholar
  21. Chavez FP., Messié M (2009) A comparison of eastern boundary upwelling ecosystems. Progr Oceanogr 83: 80–96. doi: 10.1016/j.pocean.2009.07.032
  22. Chavez FP, Bertrand A, Guevara-Carrasco R, Soler P, Csirke J (2008) The northern Humboldt Current System: Brief history, present status and a view towards the future. Progr Oceanogr 79:95–105. doi: 10.1016/j.pocean.2008.10.012
  23. Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Progr Ser 329: 281–287. doi: 10.3354/meps329281
  24. Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115. doi: 10.1086/425202 CrossRefGoogle Scholar
  25. Cherel Y, Fontaine C, Richard P, Labat J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332. doi: 10.4319/lo.2010.55.1.0324 CrossRefGoogle Scholar
  26. Chouvelon T, Spitz J, Caurant F et al (2012) Enhanced bioaccumulation of mercury in deep-sea fauna from the Bay of Biscay (north-east Atlantic) in relation to trophic positions identified by analysis of carbon and nitrogen stable isotopes. Deep Sea Res Part Oceanogr Res Pap 65:113–124. doi: 10.1016/j.dsr.2012.02.010 CrossRefGoogle Scholar
  27. Choy CA, Davison PC, Drazen JC, Flynn A, Gier EJ, Hoffman JC, McClain-Counts JP, Miller TW, Popp BN, Ross SW, Sutton TT (2012) Global trophic position comparison of two dominant mesopelagic fish Families (Myctophidae, Stomiidae) using amino acid Nitrogen isotopic analyses. PLoS ONE 7(11):e50133. doi: 10.1371/journal.pone.0050133 CrossRefGoogle Scholar
  28. Christensen V, Pauly D (1992) ECOPATH II—a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol Model 61:169–185. doi: 10.1016/0304-3800(92)90016-8
  29. Costalago D, Navarro J, Álvarez-Calleja I, Palomera I (2012) Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Mar Ecol Progr Ser 460:169–181. doi: 10.3354/meps09751
  30. Décima M, Landry MR, Popp BN (2013) Environmental perturbation effects on baseline δ15N values and zooplankton trophic flexibility in the southern California Current Ecosystem. Limnol Oceanogr 58:624–634. doi: 10.4319/lo.2013.58.2.0624 CrossRefGoogle Scholar
  31. Demarcq H (2009) Trends in primary production, sea surface temperature and wind in upwelling systems (1998–2007). Progr Oceanogr 83:376–385. doi: 10.1016/j.pocean.2009.07.022
  32. Espinoza P, Bertrand A (2008) Revisiting Peruvian anchovy (Engraulis ringens) trophodynamics provides a new vision of the Humboldt Current system. Progr Oceanogr 79:215–227. doi: 10.1016/j.pocean.2008.10.022
  33. Espinoza P, Bertrand A (2014) Ontogenetic and spatiotemporal variability in anchoveta (Engraulis ringens) diet off Peru. J Fish Biol 84(422):435. doi: 10.1111/jfb.12293 Google Scholar
  34. Espinoza P, Bertrand A, van der Lingen CD, Garrido S, Rojas de Mendiola B (2009) Diet of sardine (Sardinops sagax) in the northern Humboldt Current system and comparison with the diets of clupeoids in this and other eastern boundary upwelling systems. Progr Oceanogr 83:242–250. doi: 10.1016/j.pocean.2009.07.045
  35. Fuenzalida R, Schneider W, Garcés-Vargas J, Bravo L, Lange C (2009) Vertical and horizontal extension of the oxygen minimum zone in the eastern South Pacific Ocean. Deep Sea Res II(56):992–1003. doi: 10.1016/j.dsr2.2008.11.001 CrossRefGoogle Scholar
  36. Gallardo VA, Bustos E, Acuña A, Díaz L, Erbs V, Meléndez R, Oviedo L (1980) Relaciones ecológicas de las comunidades bentónicas y bentodemersales de la plataforma continental de Chile central. Informe División de Asistencia Técnica, Dirección de Investigaciones. Univ Concepción, Subsecretaria de pesca, p 325Google Scholar
  37. Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace movements and foraging behaviour 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-Verlag, Berlin, pp 299–318. doi: 10.1007/978-90-481-3354-3_14 Google Scholar
  38. Gutiérrez M, Ramirez A, Bertrand S, Morón O, Bertrand A (2008) Ecological niches and areas of overlap of the squat lobster ‘munida’ (Pleuroncodes monodon) and anchoveta (Engraulis ringens) off Peru. Progr Oceanogr 79:256–263. doi: 10.1016/j.pocean.2008.10.019
  39. Gutiérrez D, Sifeddine A, Field DB, Ortlieb L, Vargas G, Chávez FP, Velazco F, Ferreira V, Tapia P, Salvatteci R, Boucher H, Morales MC, Valdés J, Reyss J-L, Campusano A, Boussafir M, Mandeng-Yogo M, García M, Baumgartner T (2009) Rapid reorganization in ocean biogeochemistry off Peru towards the end of the Little Ice Age. Biogeosciences 6:835–848. doi: 10.5194/bg-6-835-2009 CrossRefGoogle Scholar
  40. Hill JM, McQuaid CD, Kaehler S (2006) Biogeographic and nearshore-offshore trends in isotope ratios of intertidal mussels and their food sources around the coast of southern Africa. Mar Ecol Progr Ser 318:63–73. doi: 10.3354/meps318063
  41. 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. doi: 10.1139/f95-209 CrossRefGoogle Scholar
  42. 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. doi: 10.1139/z97-799 CrossRefGoogle Scholar
  43. Hobson KA, Fisk A, Karnovsky N, Holst M, Gagnon JM, Fortier M (2002) A stable isotope (δ13C,δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep-Sea Res Part II 49:5131–5150. doi: 10.1016/S0967-0645(02)00182-0
  44. Hückstädt LA, Rojas CP, Antezana T (2007) Stable isotope analysis reveals pelagic foraging by the Southern sea lion in central Chile. J Exp Mar Biol Ecol 347:123–133. doi: 10.1016/j.jembe.2007.03.014 CrossRefGoogle Scholar
  45. Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250. doi: 10.1111/ele.12226 CrossRefGoogle Scholar
  46. Iitembu JA, Miller TW, Ohmori K, Kanime A, Wells S (2012) Comparison of ontogenetic trophic shift in two hake species, Merluccius capensis and Merluccius paradoxus, from the Northern Benguela Current ecosystem (Namibia) using stable isotope analysis. Fish Oceanogr 21:215–225. doi: 10.1111/j.1365-2419.2012.00614.x CrossRefGoogle Scholar
  47. Jacob U, Mintenbeck K, Brey T, Knust R, Beyer K (2005) Stable isotope food web studies: a case for standardized sample treatment. Mar Ecol Prog Ser 287:251–253. doi: 10.3354/meps287251 CrossRefGoogle Scholar
  48. Jahncke J, García-Godos A, Goya E (1997) Dieta del guanay Leucocarbo boougainvilii, del piquero peruano Sula variegata y otras aves de la costa peruana en abril y mayo de 1997. Inf Inst Mar Perú 126:75–88Google Scholar
  49. Kalvelage T, Lavik G, Lam P, Contreras S, Arteaga L, Löscher CR, Oschlies A, Paulmier A, Stramma L, Kuypers MMM (2013) Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nature Geosci 6: 228–234. doi: 10.1038/ngeo1739
  50. Kucas ST (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific southwest)—northern anchovy. US Fish Wildl. Serv. Biol. Rep. 82(11.50). U.S. Army Corps of Engineers TR EL-82-4, p 11Google Scholar
  51. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106:4752–4757. doi: 10.1073/pnas.0812444106 CrossRefGoogle Scholar
  52. Longhurst AR, Lorenzen CJ, Thomas WH (1967) The role of pelagic crabs in the grazing of phytoplankton off Baja California. Ecology 48:190–200. doi: 10.2307/1933100 CrossRefGoogle Scholar
  53. Lorrain A, Argüelles J, Alegre A, Bertrand A, Munaron J-M, Richard P, Cherel Y (2011) Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of jumbo squid (Dosidicus gigas). PLoS One 6(7):e22194. doi: 10.1371/journal.pone.0022194 CrossRefGoogle Scholar
  54. Lorrain A, Graham BS, Popp BN, Allain V, Olson RJ, Hunt BPV, Potier M, Fry B, Galván- Maga, ña F, Menkes C, Kaehler S, Ménard F (2015). Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep Sea Res Part II 113:188–198. doi: 10.1016/j.dsr2.2014.02.003
  55. Majluf P (1989) Reproductive ecology of South American fur seals in Peru. In: Pauly D, Muck P, Mendo J, Tsukayama I (eds) The Peruvian upwelling ecosystem: dynamics and interactions. ICLARM Conference Proceedings, vol 18, pp 332–343Google Scholar
  56. Medina M, Arancibia H, Neira S (2007) Un modelo trófico preliminar del ecosistema pelágico del norte de Chile (18°20′S-24°00′S). Invest Mar 35: 25–38.doi: 10.4067/S0717-71782007000100003
  57. Ménard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol 153:141–152. doi: 10.1007/s00227-007-0789-7 CrossRefGoogle Scholar
  58. Miller TW, Brodeur RD, Rau GH (2008) Carbon stable isotopes reveal relative contribution of shelf-slope production to the northern California Current pelagic community. Limnol Oceanogr 53:1493–1503. doi: 10.4319/lo.2008.53.4.1493 CrossRefGoogle Scholar
  59. Miller TW, Brodeur RD, Rau G, Omori K (2010) Prey dominance shapes trophic structure of the northern California Current pelagic food web: evidence from stable isotopes and diet analysis. Mar Ecol Progr Ser 420:15–26. doi: 10.3354/meps08876
  60. Miller TW, Bosley KL, Shibata J et al (2013) Contribution of prey to Humboldt squid Dosidicus gigas in the northern California Current, revealed by stable isotope analyses. Mar Ecol Prog Ser 477:123–134CrossRefGoogle Scholar
  61. Mollier-Vogel E, Ryabenko E, Martinez P, Wallace D, Altabet MA, Schneider R (2012) Nitrogen isotope gradients off Peru and Ecuador related to upwelling, productivity, nutrient uptake and oxygen deficiency. Deep Sea Res I(70):14–25. doi: 10.1016/j.dsr.2012.06.003 CrossRefGoogle Scholar
  62. Muck P (1989) Major trends in the pelagic ecosystem off Peru and their implications for management. In: Pauly D, Muck P, Mendo J, Tsukayama I (eds) The Peruvian upwelling ecosystem: dynamics and interactions. ICLARM Conference Proceedings, vol 18, pp 386–403Google Scholar
  63. Naqvi SWA, Naik H, Pratihary A, D’Souza W, Narvekar PV, Jayakumar DA, Devol AH, Yoshinari T, Saino T (2006) Coastal versus open-ocean denitrification in the Arabian Sea. Biogeosciences 3:621–633. doi: 10.5194/bg-3-621-2006 CrossRefGoogle Scholar
  64. Neira S, Arancibia H (2004) Trophic interactions and community structure in the Central Chile marine ecosystem (33–39°S). J Exp Mar Biol Ecol 312:349–366. doi: 10.1016/j.jembe.2004.07.011 CrossRefGoogle Scholar
  65. Olson RJ, Popp BN, Graham BS, López-Ibarra GA, Galván- Maga, ña F, Lennert-Cody CE, Bocanegra-Castillo N, Wallsgrove NJ, Gier E, Alatorre-Ramírez V, Ballance LT, Fry B (2010) Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progr Oceanogr 86:124–138. doi: 10.1016/j.pocean.2010.04.026
  66. Passuni G, Barbraud C, Chaigneau A, Demarcq H, Ledesma J, Bertrand A, Castillo R, Perea A, Mori J, Viblanc V, Torres-Maita J, Bertrand S (2016) Seasonality in marine ecosystems: Peruvian seabirds, anchovy and oceanographic conditions. Ecology 97:182–193. doi: 10.1890/14-1134.1 Google Scholar
  67. Pauly D, Tsukayama I (1987) The Peruvian anchoveta and its upwelling ecosystem: three decades of change. ICLARM Stud Rev 15Google Scholar
  68. Pauly D, Jarre A, Luna S, Sambilay JR V, Rojas De Mendiola B, Alamo A (1989). On the quantity and types of food ingested by Peruvian anchoveta, 1953–1982. In: Pauly D, Muck P, Mendo J, Tsukayama I (eds) The Peruvian upwelling ecosystem: dynamics and interactions. ICLARM Conference Proceedings, vol 18, pp 109–124Google Scholar
  69. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. SpringerGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. Ruiz-Cooley RI, Gerrodette T (2012) Tracking large-scale latitudinal patterns of δ13C and δ15N along the E Pacific using epi-mesopelagic squid as indicators. Ecosphere 3:63. doi: 10.1890/ES12-00094.1 CrossRefGoogle Scholar
  72. Ruiz-Cooley RI, Garcia KY, Hetherington ED (2011) Effects of lipid removal and preservatives on carbon and nitrogen stable isotope ratios of squid tissues: implications for ecological studies. J Exp Mar Biol Ecol 407:101–107CrossRefGoogle Scholar
  73. Ryther JH (1969) Photosynthesis and fish production in the sea. Science 166:72–76. doi: 10.1126/science.166.3901.72 CrossRefGoogle Scholar
  74. Salvatecci R (2013) Multi-decadal to millennial scale variability in Oxygen Minimum Zone intensity, export production and pelagic fish abundances from marine laminated sediments off Pisco, Peru during the last 25,000 years. PhD thesis, University Pierre et Marie Curie, pp 286Google Scholar
  75. Stowasser G, Atkinson A, McGill RAR, Phillips RA, Collins MA, Pond DW (2012) Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep-Sea Res II(59–60):208–221. doi: 10.1016/j.dsr2.2011.08.004 Google Scholar
  76. Sydeman WJ, Hobson KA, Pyle P, McLaren EB (1997) Trophic relationships among seabirds in Central California: combined stable isotope and conventional dietary approach. The Condor 99:327–336. doi: 10.2307/1369938 CrossRefGoogle Scholar
  77. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. doi: 10.1007/s00265-010-1037-6 CrossRefGoogle Scholar
  78. Takai N, Hirose N, Osawa T, Hagiwara K, Kojima T, Okazaki Y, Kuwae T, Taniuchi T, Yoshihara K (2007) Carbon source and trophic position of pelagic fish in coastal waters of south-eastern Izu Peninsula, Japan, identified by stable isotope analysis. Fish Sci 73:593–608. doi: 10.1111/j.1444-2906.2007.01372.x
  79. Tam J, Purca S, Duarte LO, Blaskovic´ V, Espinoza P (2006) Changes in the diet of hake associated with El Niño 1997–1998 in the northern Humboldt Current ecosystem. Adv Geosci 6:63–67. doi: 10.5194/adgeo-6-63-2006
  80. Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37. doi: 10.1007/BF00379558 CrossRefGoogle Scholar
  81. Tudela S, Palomera I, Quílez G (2002) Feeding of anchovy Engraulis encrasicolus larvae in the north-west Mediterranean. J Mar Biol Ass UK 82:349–350. doi: 10.1017/S0025315402005568 CrossRefGoogle Scholar
  82. Van der 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 CrossRefGoogle Scholar
  83. Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158. doi: 10.1139/f97-016 CrossRefGoogle Scholar
  84. Voss M, Dippner JW, Montoya JP (2001) Nitrogen isotope patterns in the oxygen-defficient waters of the Eastern Tropical North Pacific Ocean. Deep-Sea Res I(48):1905–1921. doi: 10.1016/S0967-0637(00)00110-2 CrossRefGoogle Scholar
  85. Weimerskirch H, Bertrand S, Silva J, Marques JC, Goya E (2010) Use of social information in seabirds: compass rafts indicate the heading of food patches. PLoS One 5(3):e9928. doi: 10.1371/journal.pone.0009928 CrossRefGoogle Scholar
  86. Zavalaga CB, Paredes R (1999) Foraging behaviour and diet of the guanay cormorant. S Afr J Mar Sci 21:251–258. doi: 10.2989/025776199784125980 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Pepe Espinoza
    • 1
    • 2
  • Anne Lorrain
    • 3
    Email author
  • Frédéric Ménard
    • 4
  • Yves Cherel
    • 5
  • Laura Tremblay-Boyer
    • 6
  • Juan Argüelles
    • 1
  • Ricardo Tafur
    • 1
  • Sophie Bertrand
    • 2
  • Yann Tremblay
    • 2
  • Patricia Ayón
    • 1
  • J.-M. Munaron
    • 3
  • Pierre Richard
    • 7
  • Arnaud Bertrand
    • 2
  1. 1.Instituto del Mar del PerúLimaPeru
  3. 3.IRD, LEMAR UMR 6539 IFREMER/IRD/CNRS/UBOPlouzanéFrance
  4. 4.Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIOMarseilleFrance
  5. 5.Centre d’Études Biologiques de Chizé (CEBC)UMR 7372 du CNRS-Université de La RochelleVilliers-en-boisFrance
  6. 6.Secretariat of the Pacific Community, SPCNouméa CedexNew Caledonia
  7. 7.Littoral, Environnement et SociétésUMR 7266 CNRS-Université de La RochelleLa RochelleFrance

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