Same size - same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals

Journal of Animal Ecology

Volumn 82, Issue 3, 2013, Pages 694-706

  Jeglinski, Jana W E ^a   Goetz, Kimberley T ^b   Werner, Christiane ^a,c   Costa, Daniel P ^b   Trillmich, Fritz ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Arctocephalus galapagoensis; Biologging; Foraging competition; Habitat segregation; Ontogeny; Stable isotopes; Zalophus wollebaeki

Indexed keywords

ABUNDANCE; ADULT; AGE CLASS; BODY SIZE; GPS; HABITAT STRUCTURE; INTERSPECIFIC COMPETITION; JUVENILE; NICHE; NICHE PARTITIONING; ONTOGENY; PINNIPED; POPULATION DYNAMICS; PREDATOR; RESOURCE USE; STABLE ISOTOPE; SYMPATRY;

ANIMAL; ANIMAL DISPERSAL; ARCTOCEPHALUS GALAPAGOENSIS; ARTICLE; BIOLOGGING; BODY SIZE; ECUADOR; ENVIRONMENT; FEEDING BEHAVIOR; FEMALE; FORAGING COMPETITION; GEOGRAPHIC INFORMATION SYSTEM; GROWTH, DEVELOPMENT AND AGING; HABITAT SEGREGATION; ONTOGENY; PHYSIOLOGY; POPULATION DYNAMICS; SEAL; STABLE ISOTOPES; ZALOPHUS WOLLEBAEKI;

ARCTOCEPHALUS GALAPAGOENSIS; BIOLOGGING; FORAGING COMPETITION; HABITAT SEGREGATION; ONTOGENY; STABLE ISOTOPES; ZALOPHUS WOLLEBAEKI;

ANIMAL DISTRIBUTION; ANIMALS; BODY SIZE; ECUADOR; ENVIRONMENT; FEEDING BEHAVIOR; FEMALE; FUR SEALS; GEOGRAPHIC INFORMATION SYSTEMS; POPULATION DYNAMICS; SEA LIONS;

ARCTOCEPHALUS GALAPAGOENSIS; MAMMALIA; OTARIIDAE; VERTEBRATA; ZALOPHUS WOLLEBAEKI;

EID: 84876301099     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12019     Document Type: Article

References (93)

1. Abbott, I., Abbott, L.K. & Grant, P.R. (1977) Comparative ecology of Galapagos ground finches (Geospiza Gould): evaluation of the importance of floristic diversity and interspecific competition. Ecological Monographs, 47, 151-184.
2. Adams, R.A. (1996) Size-specific resource use in juvenile little brown bats, Myotis lucifugus (Chiroptera: Vespertilionidae): is there an ontogenetic shift? Canadian Journal of Zoology, 74, 1204-1210.
3. Aguirre, L.F., Herrel, A., van Damme, R. & Matthysen, E. (2003) The implications of food hardness for diet in bats. Functional Ecology, 17, 201-212.
4. Ainley, D.G., Ballard, G. & Dugger, K.M. (2006) Competition among penguins and cetaceans reveals trophic cascades in the western Ross Sea, Antarctica. Ecology, 87, 2080-2093.
5. Alatalo, R.V., Eriksson, D.A.G., Gustafsson, L. & Larsson, K. (1987) Exploitation competition influences the use of foraging sites by tits: experimental evidence. Ecology, 68, 284-290.
6. Alava, J.J. & Salazar, S. (2006) Status and conservation of otariids in Ecuador and the Galápagos Islands. Symposium Volume Sea Lions of the World (eds A.W. Trites, S.K. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea & K.M. Wynne ), pp. 495 - 520. Alaska Sea Grant College Program, University of Alaska, Fairbanks, Alaska, USA.
7. Alexandrou, M.A., Oliveira, C., Maillard, M., McGill, R.A.R., Newton, J., Creer, S. & Taylor, M.I. (2011) Competition and phylogeny determine community structure in Müllerian co-mimics. Nature, 469, 84-88.
8. Antonelis, G.A., Stewart, B.S. & Perryman, W.F. (1990) Foraging characteristics of female northern fur seals (Callorhinus ursinus) and California sea lions (Zalophus californianus). Canadian Journal of Zoology, 68, 150-158.
9. Arnould, J.P.Y & Costa, D.P. (2006) Sea lions in drag, fur seals incognito: insights from the otariid deviants. Symposium Volume Sea Lions of the World (eds A.W. Trites, S.K. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L.D. Rea & K.M. Wynne ), pp. 111 - 125. Alaska Sea Grant College Program, University of Alaska, Fairbanks, Alaska, USA.
10. Ashmole, N.P. (1963) The regulation of numbers of tropical oceanic birds. Ibis, 103, 458-473.
11. Barlow, K.E., Boyd, I.L., Croxall, J.P., Reid, K., Staniland, I.J. & Brierley, A.S. (2002) Are penguins and seals in competition for Antarctic krill in South Georgia? Marine Biology, 140, 205-213.
12. Basset, A. & Angelis, D.L. (2007) Body size mediated coexistence of consumers competing for resources in space. Oikos, 116, 1363-1377.
13. Bearhop, S., Adams, C.E., Waldron, S., Fuller, R.A. & Macleod, H. (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology, 73, 1007-1101.
14. Begon, M., Townsend, C.R. & Harper, J.L. (2006) Ecology: From Individuals to Ecosystems, 5th edn, Blackwell, Oxford, UK.
15. Birt, V.L., Birt, T.P., Goulet, D., Cairnse, D.K. & Montevecchi, W.A. (1987) Ashmole's halo: direct evidence for prey depletion by a seabird. Marine Ecology Progress Series, 40, 205-208.
16. Boag, P.T. & Grant, P.R. (1984) Darwin's finches (Geospiza) on Isla Daphne major, Galapagos: breeding and feeding ecology in a climatically variable environment. Ecological Monographs, 54, 463-489.
17. Clarke, M.R. & Trillmich, F. (1980) Cephalopods in the diet of fur seals of the Galapagos Islands. Journal of Zoology, 190, 211-215.
18. Cody, M.L. & Diamond, J.L. (1975). Ecology and Evolution of Competitors. Harvard University Press, Oxford, Massachusetts, USA.
19. Costa, D.P. & Gales, N.J. (2003) Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecological Monographs, 73, 27-43.
20. Costa, D.P., Robinson, P.W., Arnould, J.P.Y., Harrison, A.-L., Simmons, S., Hassrick, J., Hoskins, A.J., Kirkman, S.P., Oosthuizen, H., Villegas-Amtmann, S. & Crocker, D. (2010) Accuracy of ARGOS locations of pinnipeds at sea estimated using FastLoc GPS. PLoS ONE, 5, e8677, 1-9.
21. Creel, S. & Creel, N.M. (1996) Limitations of African wild dogs by competition with larger carnivores. Conservation Biology, 10, 526-538.
22. Daunt, F., Afanasyev, V., Adam, A., Croxall, J.P. & Wanless, S. (2007) From cradle to early grave: juvenile mortality in European shags Phalacrocorax aristotelis results from inadequate development of foraging proficiency. Biology Letters, 3, 371-374.
23. Davis, J.M. & Stamps, J.A. (2004) The effect of natal experience on habitat preferences. Trends in Ecology an Evolution, 18, 411-416.
24. Dellinger, T. & Trillmich, F. (1999) Fish prey of the sympatric Galápagos fur seals and sea lions: seasonal variation and niche separation. Canadian Journal of Zoology, 77, 1204-1216.
25. DeNiro, M. & Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42, 495-506.
26. DeNiro, M. & Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45, 341-351.
27. Dobush, G.R., Ankney, C.D. & Krementz, D.G. (1985) The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Canadian Journal of Zoology, 63, 1917-1920.
28. Eccard, J.A. & Ylönen, H. (2003) Interspecific competition in small rodents: from populations to individuals. Evolutionary Ecology, 17, 423-440.
29. Elliott, K.H., Woo, K.J., Gaston, A.J., Benvenuti, S., Antonia, L.D. & Gail, K. (2009) Central-place foraging in an arctic seabird provides evidence for Storer-Ashmole's halo. The Auk, 126, 613-625.
30. Fowler, S.L., Costa, D.P. & Arnould, J.P.Y. (2007) Ontogeny of movements and foraging ranges in the Australian sea lion. Marine Mammal Science, 23, 598-614.
31. Franco-Trecu, V., Aurioles-Gamboa, D., Arim, M. & Lima, M. (2012) Prepartum and postpartum trophic segregations between sympatrically breeding female Arctocephalus australis and Otaria byronia. Journal of Mammology, 93, 514-521.
32. Geist, D.J., Fornari, D.J., Kurz, M.D., Harpp, K.S., Soule, S.A., Perfit, M.R. & Koleszar, A.M. (2006) Submarine Fernandina: magmatism at the leading edge of the Galápagos hot spot. Geochemistry Geophysics Geosystems, 7, 1-27.
33. Goldsworthy, S.D. & Page, B. (2007) A risk-assessment approach to evaluating the significance of seal bycatch in two Australian fisheries. Biological Conservation, 139, 269-285.
34. Goss-Custard, J.D. & Dit Durell, S.E.A.L.V. (1987) Age-related effects in oystercatchers, Haematopus ostralegus, feeding on mussels, Mytilus edulis I. Foraging efficiency and interference. Journal of Animal Ecology, 56, 521-536.
35. Götz, K.T., Robinson, P.W., Hobbs, R.C., Laidre, K.L., Huckstadt, L.A. & Shelden, K.E.W. (2012) Movement and dive behaviour of beluga whales in Cook Inlet, Alaska. AFSC Processed Report 2012-03. Alaska Fisheries Service Centre, NOAA, National Marine Fisheries Service, Seattle, Western Australia, Australia.
36. Grant, P.R. & Grant, B.R. (1982) Niche shifts and competition in Darwin's finches: Geospiza conirostris and congeners. Evolution, 36, 637-657.
37. Gurnell, J., Wauters, L.A., Lurz, P.W.W. & Tosi, G. (2004) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. Journal of Animal Ecology, 73, 26-35.
38. Gustafsson, L. (1987) Interspecific competition lowers fitness in collared flycatchers Ficedula albicollis: an experimental demonstration. Ecology, 68, 291-296.
39. Hardin, G. (1960) The competitive exclusion principle. Science, 131, 1292-1297.
40. Hobson, K.A. (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia, 120, 314-326.
41. Horning, M. & Trillmich, F. (1997) The ontogeny of the diving behaviour in the Galapagos fur seal. Behaviour, 134, 1211-1257.
42. Hutchinson, G.E. (1957) Concluding remarks: cold spring harbor symposium. Quantitative Biology, 22, 415-427.
43. Jeglinski, J.W.E., Mueller, B., Pörschmann, U. & Trillmich, F. (2010) Field-based age estimation of juvenile Galapagos sea lions (Zalophus wollebaeki) using morphometric measurements. Aquatic Mammals, 36, 262-269.
44. Jeglinski, J.W.E., Werner, C., Robinson, P., Costa, D.P. & Trillmich, F. (2012) Age, mass and environmental variation shape the foraging ontogeny of Galapagos sea lions. Marine Ecology Progress Series, 453, 279-296.
45. Jenkins, S.G., Partridge, S.T., Stephenson, T.R., Farley, S.D. & Robbins, C.T. (2001) Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia, 129, 336-341.
46. Juliano, S.A., Lounibos, L.P. & O'Meara, G.F. (2004) A field test for competitive effects of Aedes albopictus on A. aegypti in South Florida: differences between sites of coexistence and exclusion? Oecologia, 139, 583-593.
47. Kelly, J.F. (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology, 78, 1-27.
48. Kennedy, G.J.A. & Strange, C.D. (1986) The effects of intra- and inter-specific competition on the survival and growth of stocked juvenile Atlantic salmon, Salmo solar L., and resident trout, Salmo trutta L., in an upland stream. Journal of Fish Biology, 28, 479-489.
49. Kernohan, B.J., Gitzen, R.A. & Millspaugh, J.J. (2001) Analysis of animal space use and movements. In: Radiotracking Animal Populations. (edsJ.J. Millspaugh & J.M. Marzluff ), pp. 125-166. Academic Press, San Diego, USA.
50. Kie, J.G., Matthiopolous, J., Fieberg, J., Powell, R.A., Cagnacci, F., Mitchel, M.S., Gaillard, J.-M. & Moorcroft, P.R. (2010) The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philosophical Transactions of the Royal Society B, 365, 2221-2231.
51. Kooyman, G.L. (1989) Diverse Divers: Physiology and Behaviour. Springer Verlag, Berlin.
52. Kooyman, G.L. & Trillmich, F. (1986a) Diving behavior of Galápagos fur seals. In: Fur Seals: Maternal Strategies on Land and at Sea (edsR.L. Gentry & G.L. Kooyman ), pp. 186-195. Princeton University Press, Princeton, New Jersey, USA.
53. Kooyman, G.L. & Trillmich, F. (1986b) Diving behavior of Galápagos sea lions. In: Fur Seals: Maternal Strategies on Land and at Sea (edsR.L. Gentry & G.L. Kooyman ), pp. 209-219. Princeton University Press, Princeton, New Jersey, USA.
54. Kuhn, C. E., Tremblay, Y., Ream, R.R. & Gelatt, T.S. (2010) Coupling GPS tracking with dive behaviour to examine the relationship between foraging strategy and fine-scale movements of northern fur seals. Endangered Species Research, 12, 125-139.
55. Kurle, C.M. & Worthy, G.A.J. (2002) Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Marine Ecology Progress Series, 236, 289-300.
56. La Croix, S., Zelditch, M.L., Shivik, J.A.A., Lundrigan, B.L. & Holekamp, K.E. (2011) Ontogeny of feeding performance and biomechanics in coyotes. Journal of Zoology, 285, 2301-2315.
57. Lewis, S., Sherratt, T.N., Hamer, K.C. & Wanless, S. (2001) Evidence for intra-specific competition for food in a pelagic seabird. Nature, 412, 816-819.
58. Masello, J.F., Mundry, R., Poisbleau, M., Demogin, L., Voight, C.C., Wikelski, M. & Quillfeldt, P. (2010) Diving seabirds share forging space and time within and among species. Ecosphere, 1, 1-28.
59. Merlen, G. (2000) Nocturnal acoustic location of the Galapagos fur seal. Marine Mammal Science, 16, 248-253.
60. Minagawa, M. & Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta, 48, 1135-1140.
61. Mori, Y. (2002) Optimal diving behaviour for foraging in relation to body size. Journal of Evolutionary Biology, 15, 269-276.
62. Mueller, B., Pörschmann, U., Wolf, J.B.W. & Trillmich, F. (2011) Growth under uncertainty: the influence of marine variability on early development of Galapagos sea lions. Marine Mammal Science, 27, 350-365.
63. Newsome, S.D., Clementz, M.T. & Koch, P.L. (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science, 26, 509-572.
64. Newsome, S.D., Martinez del Rio, C., Bearhop, S. & Phillips, D.L. (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment, 5, 429-436.
65. Noren, SR., Biedenbach, G. & Edwards, EF. (2006) Ontogeny of swim performance and mechanics in bottlenose dolphins (Tursiops truncatus). Journal of Experimental Biology, 209, 4724-4731.
66. Paéz-Rosas, D., Aurioles-Gamboa, D., Alava, J.-J. & Palacios, D. (2012) Stable isotopes indicate differing foraging strategies in two sympatric pinnipeds of the Galapagos Islands. Journal of Experimental Marine Biology and Ecology, 424-425, 44-52.
67. Phillipps, D.L. & Gregg, J.W. (2001) Uncertainty in source partitioning using stable isotopes. Oecologia, 127, 171-179.
68. Polis, G.A. (1984) Age structure component of niche width and intraspecific resource partitioning: can age groups function as ecological species? The American Naturalist, 123, 541-564.
69. Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83, 703-718.
70. R development Core Team (2010) R: a language and environment for statistical computing.
71. Recher, B.Y.H.F. & Recher, J.A. (1969) Comparative foraging efficiency of adult and immature little blue herons (Florida caerulea). Animal Behaviour, 17, 320-322.
72. Riedmann, M. (1990) The Pinnipeds: Seals, Sea Lions and Walruses. University of California Press, Berkeley.
73. Rutten, A.L., Oosterbeek, K., Verhulst, S., Dingemanse, N.J. & Ens, B.J. (2010) Experimental evidence for interference competition in oystercatchers, Haematopus ostralegus. II. Free-living birds. Behavioural Ecology, 21, 1261-1270.
74. Schoener, T.W. (1968) The anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49, 704-726.
75. Schoener, T.W. (1983) Field experiments on interspecific competition. The American Naturalist, 122, 240-285.
76. Schreer, J.F., Kovacs, K.M. & O'Hara Hines, R.J. (2001) Comparative diving patterns of pinnipeds and seabirds. Ecological Monographs, 71, 137-162.
77. Shealer, D.A. & Burger, J. (1993) Effects of interference competition on the foraging activity of tropical Roseate terns. The Condor, 95, 322-329.
78. Simmons, S.E., Crocker, D.E., Kudela, R.M. & Costa, D.P. (2007) Linking foraging behaviour of the northern elephant seal with oceanography and bathymetry at mesoscales. Marine Ecology Progress Series, 346, 265-275.
79. Sol, D., Santos, D.M., Garcia, J. & Cuadrado, M. (1998) Competition for food in urban pigeons: the costs of being juvenile. The Condor, 100, 298-304.
80. Storer, R.W. (1952) A comparison of variation, behaviour and evolution in the sea bird genera Uria and Cepphus. University of California Publications in Zoology, 52, 121-222.
81. Subalusky, A.L., Fitzgerald, L.A. & Smith, L.L. (2009) Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems. Biological Conservation, 142, 1507-1514.
82. Thornton, A. (2008) Early body condition, time budgets and the acquisition of foraging skills in meerkats. Animal Behaviour, 75, 951-962.
83. Tremblay, Y., Shaffer, S.A., Fowler, S.L., Kuhn, C.E., McDonald, B.I., Weise, M.J., Bost, C.-A., Weimerskirch, H., Crocker, D.E., Goebel, M.E. & Costa, D.P. (2006) Interpolation of animal tracking data in a fluid environment. Journal of Experimental Biology, 209, 128-140.
84. Waite, J.N., Trumble, S.T., Burkanov, V.N. & Andrews, R.D. (2012) Resource partitioning by sympatric Steller sea lions and northern fur seals as revealed by biochemical dietary analyses and satellite telemetry. Journal of Experimental Marine Biology and Ecology, 4, 416-417, 416-417, 41-54.
85. Wauters, L.A., Lurz, P.W.W. & Gurnell, J. (2000) Interspecific effects of grey squirrels (Sciurus carolinensis) on the space use and population demography of red squirrels (Sciurus vulgaris) in conifer plantations. Ecological Research, 15, 271-284.
86. Weathers, W.W. & Sullivan, K.A. (1989) Juvenile foraging proficiency, parental effort, and avian reproductive success. Ecological Monographs, 59, 223-246.
87. Weathers, W.W. & Sullivan, K.A. (1991) Foraging efficiency of parent Juncos and their young. The Condor, 93, 346-353.
88. Weise, M.J., Harvey, J.T. & Costa, D.P. (2010) The role of body size in individual-based foraging strategies of a top marine predator. Ecology, 91, 1004-1015.
89. Werner, E.E. & Gilliam, J.F. (1984) The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics, 15, 393-425.
90. Wikelski, M., Gall, B. & Trillmich, F. (1993) Ontogenetic changes in food intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus, Bell). Oecologia, 94, 373-379.
91. Wikelski, M. & Trillmich, F. (1994) Foraging strategies of the Galapagos Marine Iguana (Amblyrhynchus cristatus): adapting behavioral rules to ontogenetic size change. Oecologia, 128, 255-279.
92. Wilson, R.P. (2010) Resource partitioning and niche hyper-volume overlap in free-living Pygoscelid penguins. Functional Ecology, 24, 646-657.
93. Wolf, J.B.W., Harrod, C., Brunner, S., Salazar, S., Trillmich, F. & Tautz, D. (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations. BMC Evolutionary Biology, 8, 150.