Marine Biology

, 165:86 | Cite as

Diversification of foraging habits among Guadalupe fur seals from their only well-established breeding colony, Guadalupe Island, Mexico

  • Ariadna Juárez-Ruiz
  • Fernando R. Elorriaga-Verplancken
  • Xchel G. Moreno-Sánchez
  • Sergio Aguíniga-García
  • María José Amador-Capitanachi
  • Casandra Gálvez
Original paper


Intra-population resource partitioning is a foraging strategy that could minimize intra-specific competition. This behavior may be ecologically relevant for species in recovery like the Guadalupe fur seal Arctocephalus philippii townsendi (GFS), which was considered extinct 70–80 years ago. The present study provides, via scat and stable isotope (δ15N and δ13C) analyses, trophic knowledge around GFSs from Guadalupe Island just prior to and the 2013 breeding season, with emphasis on inter-individual variability. A total of 107 scat samples were analyzed, and 98 neonate fur samples (proxies for adult female foraging) were isotopically assessed. The overall trophic spectrum included 12 items, with a slight increase in diversity among main prey during the second half of the breeding season. The isotopic analysis revealed three distinct groups, reflecting apparent variations in trophic position and coastal/oceanic habitat use. As in previous studies, a mostly teutophagous diet was clear; however, our work is the first to identify inter-individual prey and habitat partitioning. Based on our results and those of other studies, GFSs exhibited an opportunistic foraging strategy across the breeding season. Both analyses were complementary in terms of diversification and useful for the understanding GFS foraging strategies, which are relevant to evaluating population recovery as factors such as prey availability is suggested to be critical to this species recovery.



We thank the Secretaría de Medio Ambiente y Recursos Naturales through the Dirección General de Vida Silvestre en México for granting us research permit SGPA/DGVS/11744/13, as well as Comisión Nacional de Áreas Naturales Protegidas (CONANP)– Reserva de la Biósfera Isla Guadalupe. We also thank Secretaría de Marina (SEMAR; Mexican Navy) and the Cooperativa pesquera “Abuloneros y Langosteros de Isla Guadalupe” (fishermen society in Guadalupe Island), for their support in the field. FREV and XGMS thank IPN for the received support through the Contracting Excellence Program and fellowship EDI. We also thank Kristin Sullivan for editing the English version of the manuscript.

Compliance with ethical standards


Financial support was provided by CONACYT Cencia Básica- Project 181876 and SIP-20130944 from Instituto Politécnico Nacional (IPN).

Conflict of interest

The authors declare that they have no conflict of interest, of any kind.

Human and animal rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.


  1. Amador-Capitanachi MJ, Moreno-Sánchez XG, Juárez-Ruiz A, Ferretto G, Elorriaga-Verplancken FR (2017) Trophic variation between the two existing Guadalupe fur seal colonies on Guadalupe Island and the San Benito Archipelago, Mexico. Aquat Mammal 43:14–25. CrossRefGoogle Scholar
  2. Amador-Capitanachi MJ (2018) Nicho isotópico interanual (2013-2016) y análisis del desplazamiento mediante telemetría en el lobo fino de Guadalupe (Arctocephalus philippii townsendi). MSc dissertation. CICIMAR-IPN, La Paz, BCS, MexicoGoogle Scholar
  3. Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. J Fish Biol 48:607–614. CrossRefGoogle Scholar
  4. Arim M, Naya DE (2003) Pinniped diets inferred from scats: analysis of biases in prey occurrence. Can J Zool 81:67–73. CrossRefGoogle Scholar
  5. Aurioles-Gamboa D, Camacho-Ríos FJ (2007) Diet and feeding overlap of two Otariids, Zalophus californianus and Arctocephalus townsendi: implications to survive environmental uncertainty. Aquat Mammal 33:315–326. CrossRefGoogle Scholar
  6. Aurioles-Gamboa D, Elorriaga-Verplancken FR, Hernández CJ (2010) The current population status of Guadalupe fur seal (Arctocephalus townsendi) on the San Benito Islands, Mexico. Mar Mammal Sci 26:402–408. CrossRefGoogle Scholar
  7. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey C, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. CrossRefPubMedGoogle Scholar
  8. Boltnev AL, York AE (2001) Maternal investment in northern fur seals (Callorhinus ursinus): interrelationships among mothers’ age, size, parturition date, offspring size and sex ratios. J Zool (London) 254:219–228. CrossRefGoogle Scholar
  9. Bowen WD (2000) Reconstruction of pinniped diets: accounting for complete digestion of otoliths and cephalopod beaks. Can J Fish Aquat Sci 57:898–905. CrossRefGoogle Scholar
  10. Burton RK, Koch PL (1999) Isotopic tracking of foraging and longdistance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585. CrossRefPubMedGoogle Scholar
  11. Carlisle AB, Goldman KJ, Litvi SY, Madigan DJ, Bigman JS, Swithenbank AM, Kline TC, Block BA (2015) Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark. Proc R Soc B 282:20141446. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Casper RM, Gales NJ, Hindell MA, Robinson SM (2006) Diet estimation based on an integrated mixed prey feeding experiment using Arctocephalus seals. J Exp Mar Bio Ecol 328:228–239. CrossRefGoogle Scholar
  13. 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:e50133. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Christensen V, Pauly D (1992) ECOPATH II—a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol Modell 61:169–185. CrossRefGoogle Scholar
  15. Clarke KR, Gorley RN (2006) PRIMER v6 User Manual/Tutorial. Primer-E, Plymouth, UKGoogle Scholar
  16. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples: user’s guide and application. Accessed 13 Jan 2015
  17. da Silva J, Neilson DL (1985) Limitations of using otoliths recovered in scats to estimate prey consumption in seals. J Fish Aquat Sci 42:1439–1442. CrossRefGoogle Scholar
  18. Dellinger T, Trillmich F (1988) Estimating diet composition from scat analysis in otariid seals (Otariidae): is it reliable? Can J Zool 66:1865–1870. CrossRefGoogle Scholar
  19. DeNiro MJ, Epstein S (1981) Influence of the diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–353. CrossRefGoogle Scholar
  20. Denis V, Lejeune L, Robin JP (2002) Spatio-temporal analysis of commercial trawler data using General Additive models: patterns of Loliginid abundance in the north-east Atlantic. ICES J Mar Sci 59:633–648. CrossRefGoogle Scholar
  21. Elorriaga-Verplancken F, Aurioles-Gamboa D, Newsome SD, Martínez-Díaz SF (2013) δ15N and δ13C values in dental collagen as a proxy for age- and sex-related variation in foraging strategies of California sea lions. Mar Biol 160:641–652. CrossRefGoogle Scholar
  22. Elorriaga-Verplancken FR, Sierra-Rodríguez G, Rosales-Nanduca H, Acevedo-Whitehouse K, Sandoval-Sierra J (2016a) Impact of the 2015 El Niño-Southern Oscillation on the abundance and foraging habits of Guadalupe fur seals and California sea lions from the San Benito Archipelago, Mexico. PLoS One 11:e0155034. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Elorriaga-Verplancken FR, Juárez-Ruiz A, Baleytó MA, Galván-Magaña F, Aguíñiga-Farcía S (2016b) Isotopic variation between adult female Guadalupe fur seals and their offspring: implications for the use of neonates as proxies for maternal foraging. Aquat Mammal 42:268–276. CrossRefGoogle Scholar
  24. Esperón Rodriguez M, Gallo-Reynoso JP (2012) Analysis of the recolonization of San Benito Archipelago by Guadalupe fur seals (Arctocephalus townsendi). Lat Am J Aquat Res 40:213–223. CrossRefGoogle Scholar
  25. Estes JA, Riedman ML, Staedler MM, Tinker MT (2003) Individual variation in prey selection by sea otters: Patterns, causes and implications. J Anim Ecol 72:144–155. CrossRefGoogle Scholar
  26. Field JC, Baltz KEN, Walker W (2007) Range expansion and trophic interactions of the Jumbo Squid, Dosidicus Gigas, in the California current. Calif Coop Ocean Fish Investig Rep 48:131–146Google Scholar
  27. Fiscus CH (1982) Predation by marine mammals on squids of the eastern North Pacific Ocean and the Bering Sea. Mar Fish Rev 44:1–10Google Scholar
  28. Froese F, Pauly D (2015) Accessed 12 Apr 2015
  29. Gallo-Reynoso JP (1994) Factors affecting the population status of Guadalupe Fur Seal, Arctocephalus Townsendi (Merriam 1897) at Isla De Guadalupe, Baja California, Mexico. PhD Dissertation, University of California, Santa Cruz, CaliforniaGoogle Scholar
  30. Gallo-Reynoso JP, Esperón-Rodríguez M (2013) Diet composition of the Guadalupe fur seal (Arctocephalus townsendi). Where and what do they eat? Mar Freshw Behav Physiol 46:455–467. CrossRefGoogle Scholar
  31. Gallo-Reynoso JP, Le Boeuf BJ, Figueroa-Carranza AL, Maravilla-Chávez O (2005) Los pinnípedos de Isla Guadalupe. In: Peters E (ed) Santos del Prado K. Instituto Nacional de ecología, SEMARNAT, Mexico City, pp 171–201Google Scholar
  32. Gallo-Reynoso JP, Figueroa-Carranza AL, Le Boeuf BJ (2008) Foraging behavior of lactating Guadalupe fur seal females. In: Espinoza E, Ortega J (eds) Lorenzo C. Advances in the study of mammals in Mexico, Mexico City, pp 595–614Google Scholar
  33. García-Capitanachi B, Schramm Y, Heckel G (2017) Population Fluctuations of Guadalupe Fur Seals (Arctocephalus philippii townsendi) Between the San Benito Islands and Guadalupe Island, Mexico, During 2009 and 2010. Aquat Mammals 43(5):492–500CrossRefGoogle Scholar
  34. García-Rodríguez F, De La Cruz-Agüero J (2011) A comparison of indexes for prey importance inferred from otoliths and cephalopod beaks recovered from pinniped scats. J Fish Aquat Sci 6:186–193.
  35. Gerking SD (1994) Feeding ecology of fish. Academic, San DiegoGoogle Scholar
  36. 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. CrossRefGoogle Scholar
  37. Hanni KD, Long DJ, Jones RE, Pyle P, Morgan LE (1997) Sightings and strandings of Guadalupe Fur seals in Central and Northern California, 1988–1995. J Mammal 78:684–690. CrossRefGoogle Scholar
  38. Hernández J (2009) Distribución, abundancia y estructura alimentaria del lobo fino de Guadalupe (Arctocephalus townsendi) en Isla Guadalupe, México. MSc dissertation, Centro de Investigación Científica y Educación Superior de Ensenada, Ensenada Baja California, MexicoGoogle Scholar
  39. Hobson KA, Welch HE (1992) Determination of trophic relationships within a high arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18CrossRefGoogle Scholar
  40. 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. CrossRefGoogle Scholar
  41. Hoskins AJ, Costa DP, Wheatley KE, Gibbens JR, Arnould JPY (2015) Influence of intrinsic variation on foraging behaviour of adult female Australian fur seals. Mar Ecol Prog Ser 526:227–238. CrossRefGoogle Scholar
  42. Hubbs CL (1956) The Guadalupe fur seal still lives! Zoonooz 29:6–9Google Scholar
  43. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. Anim Ecol 80:595–602. CrossRefGoogle Scholar
  44. Jiménez VA, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Rev Ibérica Arac 8:151–161Google Scholar
  45. Kernaléguen L, Arnould JPY, Guinet C, Cherel Y (2015) Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals. J Anim Ecol 84:1081–1091. CrossRefPubMedGoogle Scholar
  46. Kintisch E (2015) “The Blob” invades Pacific, flummoxing climate experts. Science. CrossRefPubMedGoogle Scholar
  47. Krebs C (1999) Ecological methodology, 2nd edn. Addison-Wesley Educational Publishers Inc, Menlo ParkGoogle Scholar
  48. Kurle CM, Worthy GAJ (2001) Stable isotope assessment of temporal and geographic differences in feeding ecology of northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126:254–265. CrossRefPubMedGoogle Scholar
  49. Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50:324–340. CrossRefGoogle Scholar
  50. Lander M (2000) Satellite tracking a rehabilitated Guadalupe fur seal (Arctocephalus townsendi). Aquat Mammal 26:137–142Google Scholar
  51. Lewis R, O’Connell TC, Lewis M, Campagna C, Hoelzel AR (2006) Sex-specific foraging strategies and resource partitioning in the Southern elephant seals (Mirounga leonina). Proc R Soc B 273:2901–2907. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lowry MS (2011) Photographic catalog of California marine fish otoliths: prey of California sea lions (Zalophus californianus) (NMFSTechnical Memorandum) NOAA, pp 256Google Scholar
  53. Lowther AD, Harcourt RG, Page B, Goldsworthy SD (2013) Steady as he goes: at-sea movement of adult male Australian sea lions in a dynamic marine environment. PLoS One 8:e74348. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lunn NJ, Boyd IL (1993) Effects of maternal age and condition on parturition and the perinatal period of Antarctic fur seals. J Zool 229:55–67. CrossRefGoogle Scholar
  55. Markaida U, Sosa-Nishizaki O (2003) Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. J Mar Biol Assoc UK 83:507–522. CrossRefGoogle Scholar
  56. McClatchie S, Field J, Thompson AR, Gerrodette T, Lowry M, Fiedler PC, Nieto KM, Vetter RD (2016) Food limitation of sea lion pups and the decline of forage off central and southern California. R Soc Open Sci 3:150628. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mearns A, Olson R, Young D, Schafer H (1981) Trophic structure and the cesium-potassium ratio in pelagic ecosystems. CalCOFI Rep 22:99–110Google Scholar
  58. Minagawa M, Wada E (1984) Stepwise enrichment of N along food chains: further evidence and the relation between δ15N and animal age. Geachimica Cosmochim Acta 48:1135–1140. CrossRefGoogle Scholar
  59. Morrow JE (1979) Preliminary keys to otoliths of some adult fishes of the Gulf of Alaska, Bering Sea, and Beaufort Sea (NMFS Technical Report 420) U.S. Department of Commerce, NOAA, pp 32Google Scholar
  60. Nelson JS, Espinosa-Pérez H, Findley LT, Gilbert CR, Lea RN, Mandrak NE, Williams JD (2004) Common and scientific names of fishes from the United States, Canada, and Mexico. Am Fish Soc, special publication 29Google Scholar
  61. Newsome SD, Del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436. CrossRefGoogle Scholar
  62. Orr AJ, VanBlaricom GR, DeLong RL, Cruz-Escalona VH, Newsome SD (2011) Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses. Can J Zool 89:109–122. CrossRefGoogle Scholar
  63. Pablo N (2009) Amplitud, nivel y superposición trófica de los pinnípedos de Islas San Benito, BC, México. MSc dissertation. CICIMAR IPN, La Paz, BCS, MexicoGoogle Scholar
  64. Páez-Rosas D, Aurioles-Gamboa D (2010) Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki. Mar Biol 157:2769–2781. CrossRefGoogle Scholar
  65. Palomares MLD, Pauly D (2015) World Wide Web electronic publication. Accessed 14 Feb 2015
  66. Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481. CrossRefGoogle Scholar
  67. Pierce GJ, Boyle PR (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanogr Mar Biol 29:409–486Google Scholar
  68. Porras-Peters H, Aurioles-Gamboa D, Cruz-Escalona VH, Koch PL (2008) Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico. Mar Mammal Sci 24:554–576. CrossRefGoogle Scholar
  69. Post DM (2002) Using stable isotopes to estimate trophic position models methods, and assumptions. Ecology 83:703–718. CrossRefGoogle Scholar
  70. R Development Core Team (2008) R: a language and environment for statistical computing. R foundation for statistical computing. Accessed 12 Apr 2015
  71. Robson BW, Michael E, Goebel J, Ream RR, Loughlin TR, Francis RC, Costa DP et al (2004) Separation of foraging habitat among breeding sites of a colonial marine predator, the northern fur seal (Callorhinus ursinus). Can J Zool 82:20–29. CrossRefGoogle Scholar
  72. SEMARNAT, Secretaría de Medio Ambiente y Recursos Naturales (2010) Norma Oficial Mexicana NOM-059 SEMARNAT-2010. Diario Oficial de la Federación (DOF). Accessed 1 Oct 2016Google Scholar
  73. Simmons SE, Crocker DE, Kudela RM, Costa DP (2007) Linking foraging behaviour of the northern elephant seal with oceanography and bathymetry at mesoscales. Mar Ecol Prog Ser 346:265–275. CrossRefGoogle Scholar
  74. Sinclair EH, Loughlin T, Pearcy W (1994) Prey selection by northern fur seals (Callorhinus ursinus) in the eastern Bering Sea. Fish Bull 92:144–156Google Scholar
  75. Staniland IJ, Boyd IL (2003) Variation in the for-aging location of Antarctic fur seals (Arctocephalus gazella) and the effects on diving behavior. Mar Mammal Sci 19:331–343. CrossRefGoogle Scholar
  76. Stewart JS, Hazen EL, Bograd SJ, Byrnes JEK, Foley DG, Gilly WF, Robison BH, Field JC (2014) Combined climate- and prey-mediated range expansion of Humboldt squid (Dosidicus gigas), a large marine predator in the California Current System. Glob Chang Biol 20:1832–1843. CrossRefPubMedGoogle Scholar
  77. Tollit DJ, Steward MJ, Thompson PM, Pierce GJ, Santos MB, Hughes S (1997) Species and size differences in the digestion of otoliths and beaks: implications for estimates of pinniped diet composition. Can J Fish Aquat Sci 54:105–111CrossRefGoogle Scholar
  78. Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–389. CrossRefGoogle Scholar
  79. Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Velázquez CM, Elorriaga-Verplancken FR (2017) Isotopic evidence for intersexual foraging variation in northern elephant seals from Baja California. Mexico. Mar Biol 164:168. CrossRefGoogle Scholar
  81. Weber MA, Roletto J (1987) Two Recent Occurrences of the Guadalupe fur seal Arctocephalus townsendi in Central California. Bull South Calif Acad Sci 86:159–163Google Scholar
  82. Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur Seal (Arctocephalus townsendi). J Hered 95:144–153. CrossRefPubMedGoogle Scholar
  83. Wing BL (2005) Unusual invertebrates and fish observed in the Gulf of Alaska, 2004–2005. PICES Press 142:26–28Google Scholar
  84. Wolff G (1984). Identification and estimation of size from the beaks of 18 species of cephalopods from the Pacific Ocean (NMFS Technical Report 17). U.S. Department of Commerce, NOAA, Washington, DC, pp 50Google Scholar
  85. Young RE, Vecchione M, Mangold KM (2013) The tree of life web project. Accessed 28 Feb 2017

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ariadna Juárez-Ruiz
    • 1
  • Fernando R. Elorriaga-Verplancken
    • 1
  • Xchel G. Moreno-Sánchez
    • 1
  • Sergio Aguíniga-García
    • 2
  • María José Amador-Capitanachi
    • 1
  • Casandra Gálvez
    • 1
  1. 1.Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN)Departamento de Pesquerías y Biología MarinaLa PazMéxico
  2. 2.Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Departamento de OceanologíaLa PazMéxico

Personalised recommendations